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Published in: Dysphagia 5/2022

22-10-2021 | Dysphagia | Original Article

Advancing Laryngeal Adductor Reflex Testing Beyond Sensory Threshold Detection

Authors: Teresa E. Lever, Ashley M. Kloepper, Ian Deninger, Ali Hamad, Bridget L. Hopewell, Alyssa K. Ovaitt, Marlena Szewczyk, Filiz Bunyak, Bradford Zitsch, Brett Blake, Caitlin Vandell, Laura Dooley

Published in: Dysphagia | Issue 5/2022

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Abstract

Flexible endoscopic evaluation of swallowing with sensory testing (FEESST) is a promising clinical tool to assess airway integrity via the laryngeal adductor reflex (LAR). The current clinical protocol relies on sensory threshold detection, as relatively little is known about the motor response of this sensorimotor airway protective reflex. Here, we focused on characterizing normative LAR motion dynamics in 20 healthy young participants using our prototype high-pressure syringe-based air pulse device and analytic software (VFtrack™) that tracks vocal fold (VF) motion in endoscopic videos. Following device bench testing for air pulse stimulus characterization, we evoked and objectively quantified LAR motion dynamics in response to two suprathreshold air pulse stimuli (40 versus 60 mm Hg), delivered to the arytenoid mucosa through a bronchoscope working channel. The higher air pressures generated by our device permitted an approximate 1 cm endoscope working distance for continual visualization of the bilateral VFs throughout the LAR. Post hoc video analysis identified two main findings: (1) there are variant and invariant subcomponents of the LAR motor response, and (2) only a fraction of suprathreshold stimuli evoked complete glottic closure during the LAR. While the clinical relevance of these findings remains to be determined, we have nonetheless demonstrated untapped potential in the current FEESST protocol. Our ongoing efforts may reveal LAR biomarkers to quantify the severity of laryngeal pathology and change over time with natural disease progression, spontaneous recovery, or in response to intervention. The ultimate goal is to facilitate predictive modeling of patients at high risk for dysphagia-related aspiration pneumonia.
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Literature
1.
go back to reference Kaneoka A, et al. Relationship between laryngeal sensory deficits, aspiration, and pneumonia in patients with dysphagia. Dysphagia. 2018;33(2):192–9.PubMed Kaneoka A, et al. Relationship between laryngeal sensory deficits, aspiration, and pneumonia in patients with dysphagia. Dysphagia. 2018;33(2):192–9.PubMed
2.
go back to reference Wu CP, et al. National trends in admission for aspiration pneumonia in the United States, 2002–2012. Ann Am Thorac Soc. 2017;14(6):874–9.PubMed Wu CP, et al. National trends in admission for aspiration pneumonia in the United States, 2002–2012. Ann Am Thorac Soc. 2017;14(6):874–9.PubMed
3.
go back to reference Lanspa MJ, et al. Characteristics associated with clinician diagnosis of aspiration pneumonia: a descriptive study of afflicted patients and their outcomes. J Hosp Med. 2015;10(2):90–6.PubMed Lanspa MJ, et al. Characteristics associated with clinician diagnosis of aspiration pneumonia: a descriptive study of afflicted patients and their outcomes. J Hosp Med. 2015;10(2):90–6.PubMed
4.
go back to reference Lindenauer PK, et al. Variation in the diagnosis of aspiration pneumonia and association with hospital pneumonia outcomes. Ann Am Thorac Soc. 2018;15(5):562–9.PubMed Lindenauer PK, et al. Variation in the diagnosis of aspiration pneumonia and association with hospital pneumonia outcomes. Ann Am Thorac Soc. 2018;15(5):562–9.PubMed
5.
go back to reference Lanspa MJ, et al. Mortality, morbidity, and disease severity of patients with aspiration pneumonia. J Hosp Med. 2013;8(2):83–90.PubMed Lanspa MJ, et al. Mortality, morbidity, and disease severity of patients with aspiration pneumonia. J Hosp Med. 2013;8(2):83–90.PubMed
6.
go back to reference Sinclair CF, Téllez MJ, Ulkatan S. Human laryngeal sensory receptor mapping illuminates the mechanisms of laryngeal adductor reflex control. Laryngoscope. 2018;128(11):E365–70.PubMed Sinclair CF, Téllez MJ, Ulkatan S. Human laryngeal sensory receptor mapping illuminates the mechanisms of laryngeal adductor reflex control. Laryngoscope. 2018;128(11):E365–70.PubMed
7.
go back to reference Ludlow CL, et al. Abnormalities in long latency responses to superior laryngeal nerve stimulation in adductor spasmodic dysphonia. Ann Otol Rhinol Laryngol. 1995;104(12):928–35.PubMed Ludlow CL, et al. Abnormalities in long latency responses to superior laryngeal nerve stimulation in adductor spasmodic dysphonia. Ann Otol Rhinol Laryngol. 1995;104(12):928–35.PubMed
8.
go back to reference Wang B, et al. Functional regeneration of the transected recurrent laryngeal nerve using a collagen scaffold loaded with laminin and laminin-binding BDNF and GDNF. Sci Rep. 2016;6:32292.PubMedPubMedCentral Wang B, et al. Functional regeneration of the transected recurrent laryngeal nerve using a collagen scaffold loaded with laminin and laminin-binding BDNF and GDNF. Sci Rep. 2016;6:32292.PubMedPubMedCentral
9.
go back to reference Domer AS, Kuhn MA, Belafsky PC. neurophysiology and clinical implications of the laryngeal adductor reflex. Curr Otorhinolaryngol Rep. 2013;1(3):178–82.PubMedPubMedCentral Domer AS, Kuhn MA, Belafsky PC. neurophysiology and clinical implications of the laryngeal adductor reflex. Curr Otorhinolaryngol Rep. 2013;1(3):178–82.PubMedPubMedCentral
10.
go back to reference Thompson DM. Abnormal sensorimotor integrative function of the larynx in congenital laryngomalacia: a new theory of etiology. Laryngoscope. 2009;117(114):1–33. Thompson DM. Abnormal sensorimotor integrative function of the larynx in congenital laryngomalacia: a new theory of etiology. Laryngoscope. 2009;117(114):1–33.
11.
go back to reference Amin MR, et al. Sensory testing in the assessment of laryngeal sensation in patients with amyotrophic lateral sclerosis. Ann Otol Rhinol Laryngol. 2006;115(7):528–34.PubMed Amin MR, et al. Sensory testing in the assessment of laryngeal sensation in patients with amyotrophic lateral sclerosis. Ann Otol Rhinol Laryngol. 2006;115(7):528–34.PubMed
12.
go back to reference Aviv JE, et al. FEESST: a new bedside endoscopic test of the motor and sensory components of swallowing. Ann Otol Rhinol Laryngol. 1998;107(5 Pt 1):378–87.PubMed Aviv JE, et al. FEESST: a new bedside endoscopic test of the motor and sensory components of swallowing. Ann Otol Rhinol Laryngol. 1998;107(5 Pt 1):378–87.PubMed
13.
go back to reference Aviv JE, et al. Fiberoptic endoscopic evaluation of swallowing with sensory testing (FEESST) in healthy controls. Dysphagia. 1998;13(2):87–92.PubMed Aviv JE, et al. Fiberoptic endoscopic evaluation of swallowing with sensory testing (FEESST) in healthy controls. Dysphagia. 1998;13(2):87–92.PubMed
16.
go back to reference Richter GT. Supraglottic mechanics. Laryngoscope. 2012;122(Suppl 4):S80–1.PubMed Richter GT. Supraglottic mechanics. Laryngoscope. 2012;122(Suppl 4):S80–1.PubMed
17.
go back to reference Setzen M, et al. The association between laryngopharyngeal sensory deficits, pharyngeal motor function, and the prevalence of aspiration with thin liquids. Otolaryngol Head Neck Surg. 2003;128(1):99–102.PubMed Setzen M, et al. The association between laryngopharyngeal sensory deficits, pharyngeal motor function, and the prevalence of aspiration with thin liquids. Otolaryngol Head Neck Surg. 2003;128(1):99–102.PubMed
18.
go back to reference Aviv JE, et al. Laryngeal adductor reflex and pharyngeal squeeze as predictors of laryngeal penetration and aspiration. Laryngoscope. 2002;112(2):338–41.PubMed Aviv JE, et al. Laryngeal adductor reflex and pharyngeal squeeze as predictors of laryngeal penetration and aspiration. Laryngoscope. 2002;112(2):338–41.PubMed
19.
go back to reference Rees CJ. Flexible endoscopic evaluation of swallowing with sensory testing. Curr Opin Otolaryngol Head Neck Surg. 2006;14(6):425–30.PubMed Rees CJ. Flexible endoscopic evaluation of swallowing with sensory testing. Curr Opin Otolaryngol Head Neck Surg. 2006;14(6):425–30.PubMed
20.
go back to reference Allen E, Minutello K, Murcek BW. Anatomy, head and neck, larynx recurrent laryngeal nerve. 2020, StatPearls. Allen E, Minutello K, Murcek BW. Anatomy, head and neck, larynx recurrent laryngeal nerve. 2020, StatPearls.
21.
go back to reference Ulkatan S, Tellez JM, Sinclair FC. S124: Comprehensive tube-based methodology for evaluating the brainstem laryngeal adductor reflex in humans under anesthesia. Clin Neurophysiol. 2018;129:e188. Ulkatan S, Tellez JM, Sinclair FC. S124: Comprehensive tube-based methodology for evaluating the brainstem laryngeal adductor reflex in humans under anesthesia. Clin Neurophysiol. 2018;129:e188.
22.
go back to reference Kearney PR, et al. Suppression of thyroarytenoid muscle responses during repeated air pressure stimulation of the laryngeal mucosa in awake humans. Ann Otol Rhinol Laryngol. 2005;114(4):264–70.PubMedPubMedCentral Kearney PR, et al. Suppression of thyroarytenoid muscle responses during repeated air pressure stimulation of the laryngeal mucosa in awake humans. Ann Otol Rhinol Laryngol. 2005;114(4):264–70.PubMedPubMedCentral
23.
go back to reference Borders JC, et al. Inter- and intra-rater reliability of laryngeal sensation testing with the touch method during flexible endoscopic evaluations of swallowing. Ann Otol Rhinol Laryngol. 2020;129(6):565–71.PubMed Borders JC, et al. Inter- and intra-rater reliability of laryngeal sensation testing with the touch method during flexible endoscopic evaluations of swallowing. Ann Otol Rhinol Laryngol. 2020;129(6):565–71.PubMed
24.
go back to reference Langmore SE, Schatz K, Olsen N. Fiberoptic endoscopic examination of swallowing safety: a new procedure. Dysphagia. 1988;2(4):216–9.PubMed Langmore SE, Schatz K, Olsen N. Fiberoptic endoscopic examination of swallowing safety: a new procedure. Dysphagia. 1988;2(4):216–9.PubMed
25.
go back to reference Kaneoka A, et al. Variability of the pressure measurements exerted by the tip of laryngoscope during laryngeal sensory testing: a clinical demonstration. Am J Speech Lang Pathol. 2017;26(3):729–36.PubMed Kaneoka A, et al. Variability of the pressure measurements exerted by the tip of laryngoscope during laryngeal sensory testing: a clinical demonstration. Am J Speech Lang Pathol. 2017;26(3):729–36.PubMed
26.
go back to reference Link DT, et al. Pediatric laryngopharyngeal sensory testing during flexible endoscopic evaluation of swallowing: feasible and correlative. Ann Otol Rhinol Laryngol. 2000;109(10 Pt 1):899–905.PubMed Link DT, et al. Pediatric laryngopharyngeal sensory testing during flexible endoscopic evaluation of swallowing: feasible and correlative. Ann Otol Rhinol Laryngol. 2000;109(10 Pt 1):899–905.PubMed
27.
go back to reference Satoh AK. Laryngeal sensory testing using flexible endoscopy, 2016. Satoh AK. Laryngeal sensory testing using flexible endoscopy, 2016.
28.
go back to reference Langmore SE. History of fiberoptic endoscopic evaluation of swallowing for evaluation and management of pharyngeal dysphagia: changes over the years. Dysphagia. 2017;32(1):27–38.PubMed Langmore SE. History of fiberoptic endoscopic evaluation of swallowing for evaluation and management of pharyngeal dysphagia: changes over the years. Dysphagia. 2017;32(1):27–38.PubMed
29.
go back to reference Kaneoka A, et al. A comparison of 2 methods of endoscopic laryngeal sensory testing: a preliminary study. Ann Otol Rhinol Laryngol. 2015;124(3):187–93.PubMed Kaneoka A, et al. A comparison of 2 methods of endoscopic laryngeal sensory testing: a preliminary study. Ann Otol Rhinol Laryngol. 2015;124(3):187–93.PubMed
30.
go back to reference Shock LA, et al. Improving the utility of laryngeal adductor reflex testing: a translational tale of mice and men. Otolaryngol Head Neck Surg. 2015;153(1):94–101.PubMed Shock LA, et al. Improving the utility of laryngeal adductor reflex testing: a translational tale of mice and men. Otolaryngol Head Neck Surg. 2015;153(1):94–101.PubMed
31.
go back to reference Tham LK, et al. The validity and reliability of motion analysis in patellar tendon reflex assessment. PLoS ONE. 2013;8(2):e55702.PubMedPubMedCentral Tham LK, et al. The validity and reliability of motion analysis in patellar tendon reflex assessment. PLoS ONE. 2013;8(2):e55702.PubMedPubMedCentral
32.
go back to reference Jerath N, Kimura J. F wave, A wave, H reflex, and blink reflex. Handb Clin Neurol. 2019;160:225–39.PubMed Jerath N, Kimura J. F wave, A wave, H reflex, and blink reflex. Handb Clin Neurol. 2019;160:225–39.PubMed
33.
go back to reference Bergamin O, Kardon RH. Latency of the pupil light reflex: sample rate, stimulus intensity, and variation in normal subjects. Invest Ophthalmol Vis Sci. 2003;44(4):1546–54.PubMed Bergamin O, Kardon RH. Latency of the pupil light reflex: sample rate, stimulus intensity, and variation in normal subjects. Invest Ophthalmol Vis Sci. 2003;44(4):1546–54.PubMed
34.
go back to reference Bixler EO, Bartlett NR, Lansing RW. Latency of the blink reflex and stimulus intensity. J Perception Psychophys. 1967;2:559–60. Bixler EO, Bartlett NR, Lansing RW. Latency of the blink reflex and stimulus intensity. J Perception Psychophys. 1967;2:559–60.
35.
go back to reference Haney MM, et al. Automated quantification of vocal fold motion in a recurrent laryngeal nerve injury mouse model. Laryngoscope. 2019;129(7):E247–54.PubMed Haney MM, et al. Automated quantification of vocal fold motion in a recurrent laryngeal nerve injury mouse model. Laryngoscope. 2019;129(7):E247–54.PubMed
36.
go back to reference Haney MM, et al. Recurrent laryngeal nerve transection in mice results in translational upper airway dysfunction. J Comp Neurol. 2020;528(4):574–96.PubMed Haney MM, et al. Recurrent laryngeal nerve transection in mice results in translational upper airway dysfunction. J Comp Neurol. 2020;528(4):574–96.PubMed
37.
go back to reference Welby L, et al. Persistent feeding and swallowing deficits in a mouse model of 22q11.2 deletion syndrome. Front Neurol. 2020;11:4.PubMedPubMedCentral Welby L, et al. Persistent feeding and swallowing deficits in a mouse model of 22q11.2 deletion syndrome. Front Neurol. 2020;11:4.PubMedPubMedCentral
38.
go back to reference Ali Hamad A, et al. Automated segmentation of the vocal folds in laryngeal endoscopy videos using deep convolutional regression networks. In: IEEE/CVF Conference on Computer Vision and Pattern Recognition Workshops (CVPRW). Long Beach, CA: IEEE; 2019. p. 140–8. Ali Hamad A, et al. Automated segmentation of the vocal folds in laryngeal endoscopy videos using deep convolutional regression networks. In: IEEE/CVF Conference on Computer Vision and Pattern Recognition Workshops (CVPRW). Long Beach, CA: IEEE; 2019. p. 140–8.
39.
go back to reference Bielamowicz S. Aging voice or vocal fold paresis: what can I do about it? Arch Otolaryngol Head Neck Surg 2004;130(9):1114–6; discussion 118. Bielamowicz S. Aging voice or vocal fold paresis: what can I do about it? Arch Otolaryngol Head Neck Surg 2004;130(9):1114–6; discussion 118.
40.
go back to reference Aviv JE. Effects of aging on sensitivity of the pharyngeal and supraglottic areas. Am J Med. 1997;103(5A):74S-76S.PubMed Aviv JE. Effects of aging on sensitivity of the pharyngeal and supraglottic areas. Am J Med. 1997;103(5A):74S-76S.PubMed
41.
go back to reference Humbert IA, et al. Neurophysiology of swallowing: effects of age and bolus type. Neuroimage. 2009;44(3):982–91.PubMed Humbert IA, et al. Neurophysiology of swallowing: effects of age and bolus type. Neuroimage. 2009;44(3):982–91.PubMed
42.
go back to reference Rieutord M. Fluid dynamics an introduction. Graduate texts in physics. 1st ed. New York: Springer; 2015. p. 508. Rieutord M. Fluid dynamics an introduction. Graduate texts in physics. 1st ed. New York: Springer; 2015. p. 508.
43.
go back to reference Lowenstein O, Loewenfeld IE. Mutual role of sympathetic and parasympathetic in shaping of the pupillary reflex to light; pupillographic studies. Arch Neurol Psychiatry. 1950;64(3):341–77.PubMed Lowenstein O, Loewenfeld IE. Mutual role of sympathetic and parasympathetic in shaping of the pupillary reflex to light; pupillographic studies. Arch Neurol Psychiatry. 1950;64(3):341–77.PubMed
44.
go back to reference Cohen N, Moyal N, Henik A. Executive control suppresses pupillary responses to aversive stimuli. Biol Psychol. 2015;112:1–11.PubMed Cohen N, Moyal N, Henik A. Executive control suppresses pupillary responses to aversive stimuli. Biol Psychol. 2015;112:1–11.PubMed
45.
go back to reference Johnson PE, Belafsky PC, Postma GN. Topical nasal anesthesia and laryngopharyngeal sensory testing: a prospective, double-blind crossover study. Ann Otol Rhinol Laryngol. 2003;112(1):14–6.PubMed Johnson PE, Belafsky PC, Postma GN. Topical nasal anesthesia and laryngopharyngeal sensory testing: a prospective, double-blind crossover study. Ann Otol Rhinol Laryngol. 2003;112(1):14–6.PubMed
46.
go back to reference O’Dea MB, et al. Effect of lidocaine on swallowing during FEES in patients with dysphagia. Ann Otol Rhinol Laryngol. 2015;124(7):537–44.PubMed O’Dea MB, et al. Effect of lidocaine on swallowing during FEES in patients with dysphagia. Ann Otol Rhinol Laryngol. 2015;124(7):537–44.PubMed
47.
go back to reference Kamarunas EE, et al. Effects of topical nasal anesthetic on fiberoptic endoscopic examination of swallowing with sensory testing (FEESST). Dysphagia. 2014;29(1):33–43.PubMed Kamarunas EE, et al. Effects of topical nasal anesthetic on fiberoptic endoscopic examination of swallowing with sensory testing (FEESST). Dysphagia. 2014;29(1):33–43.PubMed
Metadata
Title
Advancing Laryngeal Adductor Reflex Testing Beyond Sensory Threshold Detection
Authors
Teresa E. Lever
Ashley M. Kloepper
Ian Deninger
Ali Hamad
Bridget L. Hopewell
Alyssa K. Ovaitt
Marlena Szewczyk
Filiz Bunyak
Bradford Zitsch
Brett Blake
Caitlin Vandell
Laura Dooley
Publication date
22-10-2021
Publisher
Springer US
Published in
Dysphagia / Issue 5/2022
Print ISSN: 0179-051X
Electronic ISSN: 1432-0460
DOI
https://doi.org/10.1007/s00455-021-10374-5

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