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Published in: Dysphagia 1/2017

01-02-2017 | Review

Animal Models for Dysphagia Studies: What Have We Learnt So Far

Authors: Rebecca Z. German, A. W. Crompton, Francois D. H. Gould, Allan J. Thexton

Published in: Dysphagia | Issue 1/2017

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Abstract

Research using animal models has contributed significantly to realizing the goal of understanding dysfunction and improving the care of patients who suffer from dysphagia. But why should other researchers and the clinicians who see patients day in and day out care about this work? Results from studies of animal models have the potential to change and grow how we think about dysphagia research and practice in general, well beyond applying specific results to human studies. Animal research provides two key contributions to our understanding of dysphagia. The first is a more complete characterization of the physiology of both normal and pathological swallow than is possible in human subjects. The second is suggesting of specific, physiological, targets for development and testing of treatment interventions to improve dysphagia outcomes.
Literature
1.
go back to reference Arce-McShane FI, Hatsopoulos NG, Lee JC, Ross CF, Sessle BJ. Modulation dynamics in the orofacial sensorimotor cortex during motor skill acquisition. J Neurosci. 2014;34(17):5985–97.CrossRefPubMedPubMedCentral Arce-McShane FI, Hatsopoulos NG, Lee JC, Ross CF, Sessle BJ. Modulation dynamics in the orofacial sensorimotor cortex during motor skill acquisition. J Neurosci. 2014;34(17):5985–97.CrossRefPubMedPubMedCentral
2.
go back to reference Arce-McShane FI, Ross CF, Takahashi K, Sessle BJ, Hatsopoulos NG. Primary motor and sensory cortical areas communicate via spatiotemporally coordinated networks at multiple frequencies. Proc Natl Acad Sci USA. 2016;113(18):5083–8.CrossRefPubMedPubMedCentral Arce-McShane FI, Ross CF, Takahashi K, Sessle BJ, Hatsopoulos NG. Primary motor and sensory cortical areas communicate via spatiotemporally coordinated networks at multiple frequencies. Proc Natl Acad Sci USA. 2016;113(18):5083–8.CrossRefPubMedPubMedCentral
3.
go back to reference Arce FI, Lee JC, Ross CF, Sessle BJ, Hatsopoulos NG. Directional information from neuronal ensembles in the primate orofacial sensorimotor cortex. J Neurophysiol. 2013;110(6):1357–69.CrossRefPubMed Arce FI, Lee JC, Ross CF, Sessle BJ, Hatsopoulos NG. Directional information from neuronal ensembles in the primate orofacial sensorimotor cortex. J Neurophysiol. 2013;110(6):1357–69.CrossRefPubMed
4.
go back to reference Barkmeier JM, Bielamowicz S, Takeda N, Ludlow CL. Laryngeal activity during upright vs. supine swallowing. J Appl Physiol (1985). 2002;93(2):740–5.CrossRef Barkmeier JM, Bielamowicz S, Takeda N, Ludlow CL. Laryngeal activity during upright vs. supine swallowing. J Appl Physiol (1985). 2002;93(2):740–5.CrossRef
5.
go back to reference Best MD, Nakamura Y, Kijak NA, Allen MJ, Lever TE, Hatsopoulos NG, Ross CF, Takahashi K. Semiautomatic marker tracking of tongue positions captured by videofluoroscopy during primate feeding. Conf Proc IEEE Eng Med Biol Soc. 2015;2015:5347–50.PubMedPubMedCentral Best MD, Nakamura Y, Kijak NA, Allen MJ, Lever TE, Hatsopoulos NG, Ross CF, Takahashi K. Semiautomatic marker tracking of tongue positions captured by videofluoroscopy during primate feeding. Conf Proc IEEE Eng Med Biol Soc. 2015;2015:5347–50.PubMedPubMedCentral
6.
go back to reference Blitzer A, et al. Recommendations of the neurolaryngology study group on laryngeal electromyography. Otolaryngol–Head Neck Surg. 2009;140(6):782–93.CrossRefPubMed Blitzer A, et al. Recommendations of the neurolaryngology study group on laryngeal electromyography. Otolaryngol–Head Neck Surg. 2009;140(6):782–93.CrossRefPubMed
7.
go back to reference Campbell-Malone R, Crompton AW, Thexton AJ, German RZ. Ontogenetic changes in mammalian feeding: insights from electromyographic data. Integr Comp Biol. 2011;51(2):282–8.CrossRefPubMedPubMedCentral Campbell-Malone R, Crompton AW, Thexton AJ, German RZ. Ontogenetic changes in mammalian feeding: insights from electromyographic data. Integr Comp Biol. 2011;51(2):282–8.CrossRefPubMedPubMedCentral
8.
go back to reference Ciucci MR, Russell JA, Schaser AJ, Doll EJ, Vinney LM, Connor NP. Tongue force and timing deficits in a rat model of Parkinson disease. Behav Brain Res. 2011;222(2):315–20.CrossRefPubMedPubMedCentral Ciucci MR, Russell JA, Schaser AJ, Doll EJ, Vinney LM, Connor NP. Tongue force and timing deficits in a rat model of Parkinson disease. Behav Brain Res. 2011;222(2):315–20.CrossRefPubMedPubMedCentral
10.
go back to reference Daniels SK. Letter by Daniels regarding article silent aspiration risk is volume-dependent. Dysphagia. 2012;27(2):294.CrossRefPubMed Daniels SK. Letter by Daniels regarding article silent aspiration risk is volume-dependent. Dysphagia. 2012;27(2):294.CrossRefPubMed
11.
go back to reference Ding P, Campbell-Malone R, Holman SD, Lukasik SL, Thexton AJ, German RZ. The effect of unilateral superior laryngeal nerve lesion on swallowing threshold volume. The Laryngoscope. 2013;123(8):1942–7.CrossRefPubMedPubMedCentral Ding P, Campbell-Malone R, Holman SD, Lukasik SL, Thexton AJ, German RZ. The effect of unilateral superior laryngeal nerve lesion on swallowing threshold volume. The Laryngoscope. 2013;123(8):1942–7.CrossRefPubMedPubMedCentral
12.
go back to reference Ding P, Fung GS, Lin M, Holman SD, German RZ. The effect of bilateral superior laryngeal nerve lesion on swallowing: a novel method to quantitate aspirated volume and pharyngeal threshold in videofluoroscopy. Dysphagia. 2015;30(1):47–56.CrossRefPubMed Ding P, Fung GS, Lin M, Holman SD, German RZ. The effect of bilateral superior laryngeal nerve lesion on swallowing: a novel method to quantitate aspirated volume and pharyngeal threshold in videofluoroscopy. Dysphagia. 2015;30(1):47–56.CrossRefPubMed
13.
go back to reference Fukuhara T, Tsujimura T, Kajii Y, Yamamura K, Inoue M. Effects of electrical stimulation of the superior laryngeal nerve on the jaw-opening reflex. Brain Res. 2011;1391:44–53.CrossRefPubMed Fukuhara T, Tsujimura T, Kajii Y, Yamamura K, Inoue M. Effects of electrical stimulation of the superior laryngeal nerve on the jaw-opening reflex. Brain Res. 2011;1391:44–53.CrossRefPubMed
14.
go back to reference German RZ, Crompton AW, Levitch LC, Thexton AJ. The mechanism of suckling in two species of infant mammal: miniature pigs and long-tailed macaques. J Exp Zool. 1992;261:322–30.CrossRefPubMed German RZ, Crompton AW, Levitch LC, Thexton AJ. The mechanism of suckling in two species of infant mammal: miniature pigs and long-tailed macaques. J Exp Zool. 1992;261:322–30.CrossRefPubMed
15.
go back to reference German RZ, Crompton AW, Thexton AJ. The coordination and interaction between respiration and deglutition in young pigs. J Comp Physiol (A). 1998;182:539–47.CrossRef German RZ, Crompton AW, Thexton AJ. The coordination and interaction between respiration and deglutition in young pigs. J Comp Physiol (A). 1998;182:539–47.CrossRef
16.
go back to reference Gould FD, Lammers AR, Ohlemacher J, Ballester A, Fraley L, Gross A, German RZ. The physiologic impact of unilateral recurrent laryngeal nerve (RLN) lesion on infant oropharyngeal and esophageal performance. Dysphagia. 2015;30(6):714–22.CrossRefPubMedPubMedCentral Gould FD, Lammers AR, Ohlemacher J, Ballester A, Fraley L, Gross A, German RZ. The physiologic impact of unilateral recurrent laryngeal nerve (RLN) lesion on infant oropharyngeal and esophageal performance. Dysphagia. 2015;30(6):714–22.CrossRefPubMedPubMedCentral
17.
go back to reference Hiraba H, Sato T. Cortical control for mastication in cats: changes in masticatory movements following lesions in the masticatory cortex. Somatosens Mot Res. 2005;22(3):171–81.CrossRefPubMed Hiraba H, Sato T. Cortical control for mastication in cats: changes in masticatory movements following lesions in the masticatory cortex. Somatosens Mot Res. 2005;22(3):171–81.CrossRefPubMed
18.
go back to reference Holman SD, Campbell-Malone R, Ding P, Gierbolini-Norat EM, Lukasik SL, Waranch DR, German RZ. Swallowing kinematics and airway protection after palatal local anesthesia in infant pigs. The Laryngoscope. 2013. doi:10.1002/lary.24204. Holman SD, Campbell-Malone R, Ding P, Gierbolini-Norat EM, Lukasik SL, Waranch DR, German RZ. Swallowing kinematics and airway protection after palatal local anesthesia in infant pigs. The Laryngoscope. 2013. doi:10.​1002/​lary.​24204.
19.
go back to reference Ikeda J, Kojima N, Saeki K, Ishihara M, Takayama M. Perindopril increases the swallowing reflex by inhibiting substance P degradation and tyrosine hydroxylase activation in a rat model of dysphagia. Eur J Pharmacol. 2015;746:126–31.CrossRefPubMed Ikeda J, Kojima N, Saeki K, Ishihara M, Takayama M. Perindopril increases the swallowing reflex by inhibiting substance P degradation and tyrosine hydroxylase activation in a rat model of dysphagia. Eur J Pharmacol. 2015;746:126–31.CrossRefPubMed
20.
go back to reference Inokuchi H, Gonzalez-Fernandez M, Matsuo K, Brodsky MB, Yoda M, Taniguchi H, Okazaki H, Hiraoka T, Palmer JB. Electromyography of swallowing with fine wire intramuscular electrodes in healthy human: activation sequence of selected hyoid muscles. Dysphagia. 2014;29(6):713–21.CrossRefPubMed Inokuchi H, Gonzalez-Fernandez M, Matsuo K, Brodsky MB, Yoda M, Taniguchi H, Okazaki H, Hiraoka T, Palmer JB. Electromyography of swallowing with fine wire intramuscular electrodes in healthy human: activation sequence of selected hyoid muscles. Dysphagia. 2014;29(6):713–21.CrossRefPubMed
21.
go back to reference Inokuchi H, Gonzalez-Fernandez M, Matsuo K, Brodsky MB, Yoda M, Taniguchi H, Okazaki H, Hiraoka T, Palmer JB. Electromyography of swallowing with fine wire intramuscular electrodes in healthy human: amplitude difference of selected hyoid muscles. Dysphagia. 2016;31(1):33–40.CrossRefPubMed Inokuchi H, Gonzalez-Fernandez M, Matsuo K, Brodsky MB, Yoda M, Taniguchi H, Okazaki H, Hiraoka T, Palmer JB. Electromyography of swallowing with fine wire intramuscular electrodes in healthy human: amplitude difference of selected hyoid muscles. Dysphagia. 2016;31(1):33–40.CrossRefPubMed
22.
go back to reference Kelm-Nelson CA, Yang KM, Ciucci MR. Exercise effects on early vocal ultrasonic communication dysfunction in a PINK1 knockout model of Parkinson’s disease. J Parkinsons Dis. 2015;5(4):749–63.CrossRefPubMedPubMedCentral Kelm-Nelson CA, Yang KM, Ciucci MR. Exercise effects on early vocal ultrasonic communication dysfunction in a PINK1 knockout model of Parkinson’s disease. J Parkinsons Dis. 2015;5(4):749–63.CrossRefPubMedPubMedCentral
23.
go back to reference Kelm-Nelson CA, Stevenson SA, Ciucci MR. Data in support of qPCR primer design and verification in a Pink1 -/- rat model of Parkinson disease. Data Brief. 2016;8:360–3.CrossRefPubMedPubMedCentral Kelm-Nelson CA, Stevenson SA, Ciucci MR. Data in support of qPCR primer design and verification in a Pink1 -/- rat model of Parkinson disease. Data Brief. 2016;8:360–3.CrossRefPubMedPubMedCentral
24.
go back to reference Lang IM, Dana N, Medda BK, Shaker R. Mechanisms of airway protection during retching, vomiting, and swallowing. Am J Physiol Gastrointest Liver Physiol. 2002;283(3):G529–36.CrossRefPubMed Lang IM, Dana N, Medda BK, Shaker R. Mechanisms of airway protection during retching, vomiting, and swallowing. Am J Physiol Gastrointest Liver Physiol. 2002;283(3):G529–36.CrossRefPubMed
25.
go back to reference Lang IM, Medda BK, Shaker R. Differential activation of medullary vagal nuclei caused by stimulation of different esophageal mechanoreceptors. Brain Res. 2011;1368:119–33.CrossRefPubMed Lang IM, Medda BK, Shaker R. Differential activation of medullary vagal nuclei caused by stimulation of different esophageal mechanoreceptors. Brain Res. 2011;1368:119–33.CrossRefPubMed
26.
go back to reference Lang IM, Medda BK, Jadcherla S, Shaker R. The role of the superior laryngeal nerve in esophageal reflexes. Am J Physiol Gastrointest Liver Physiol. 2012;302(12):G1445–57.CrossRefPubMedPubMedCentral Lang IM, Medda BK, Jadcherla S, Shaker R. The role of the superior laryngeal nerve in esophageal reflexes. Am J Physiol Gastrointest Liver Physiol. 2012;302(12):G1445–57.CrossRefPubMedPubMedCentral
28.
go back to reference Lever TE, Simon E, Cox KT, Capra NF, O’Brien KF, Hough MS, Murashov AK. A mouse model of pharyngeal dysphagia in amyotrophic lateral sclerosis. Dysphagia. 2010;25(2):112–26.CrossRefPubMed Lever TE, Simon E, Cox KT, Capra NF, O’Brien KF, Hough MS, Murashov AK. A mouse model of pharyngeal dysphagia in amyotrophic lateral sclerosis. Dysphagia. 2010;25(2):112–26.CrossRefPubMed
29.
go back to reference Lever TE, Brooks RT, Thombs LA, Littrell LL, Harris RA, Allen MJ, Kadosh MD, Robbins KL. Videofluoroscopic validation of a translational murine model of presbyphagia. Dysphagia. 2015;30(3):328–42.CrossRefPubMed Lever TE, Brooks RT, Thombs LA, Littrell LL, Harris RA, Allen MJ, Kadosh MD, Robbins KL. Videofluoroscopic validation of a translational murine model of presbyphagia. Dysphagia. 2015;30(3):328–42.CrossRefPubMed
30.
go back to reference Lilienfeld AM, The Fielding H. Garrison lecture: ceteris paribus: the evolution of the clinical trial. Bull Hist Med. 1982;56(1):1–18.PubMed Lilienfeld AM, The Fielding H. Garrison lecture: ceteris paribus: the evolution of the clinical trial. Bull Hist Med. 1982;56(1):1–18.PubMed
31.
32.
go back to reference Ma D, Shuler JM, Kumar A, Stanford QR, Tungtur S, Nishimune H, Stanford JA. Effects of tongue force training on bulbar motor function in the female SOD1-G93A rat model of amyotrophic lateral sclerosis. Neurorehabil Neural Repair. 2016. doi:10.1177/1545968316666956.PubMed Ma D, Shuler JM, Kumar A, Stanford QR, Tungtur S, Nishimune H, Stanford JA. Effects of tongue force training on bulbar motor function in the female SOD1-G93A rat model of amyotrophic lateral sclerosis. Neurorehabil Neural Repair. 2016. doi:10.​1177/​1545968316666956​.PubMed
33.
go back to reference Macrae PR, Jones RD, Huckabee ML. The effect of swallowing treatments on corticobulbar excitability: a review of transcranial magnetic stimulation induced motor evoked potentials. J Neurosci Methods. 2014;233:89–98.CrossRefPubMed Macrae PR, Jones RD, Huckabee ML. The effect of swallowing treatments on corticobulbar excitability: a review of transcranial magnetic stimulation induced motor evoked potentials. J Neurosci Methods. 2014;233:89–98.CrossRefPubMed
34.
go back to reference Magara J, Michou E, Raginis-Zborowska A, Inoue M, Hamdy S. Exploring the effects of synchronous pharyngeal electrical stimulation with swallowing carbonated water on cortical excitability in the human pharyngeal motor system. Neurogastroenterol Motil. 2016;28(9):1391–400.CrossRefPubMed Magara J, Michou E, Raginis-Zborowska A, Inoue M, Hamdy S. Exploring the effects of synchronous pharyngeal electrical stimulation with swallowing carbonated water on cortical excitability in the human pharyngeal motor system. Neurogastroenterol Motil. 2016;28(9):1391–400.CrossRefPubMed
35.
go back to reference Michou E, Mistry S, Jefferson S, Tyrrell P, Hamdy S. Characterizing the mechanisms of central and peripheral forms of neurostimulation in chronic dysphagic stroke patients. Brain Stimul. 2014;7(1):66–73.CrossRefPubMedPubMedCentral Michou E, Mistry S, Jefferson S, Tyrrell P, Hamdy S. Characterizing the mechanisms of central and peripheral forms of neurostimulation in chronic dysphagic stroke patients. Brain Stimul. 2014;7(1):66–73.CrossRefPubMedPubMedCentral
36.
go back to reference Morishima Y, Chida K, Watanabe H. Estimation of the dose of radiation received by patient and physician during a videofluoroscopic swallowing study. Dysphagia. 2016;31(4):574–8.CrossRefPubMed Morishima Y, Chida K, Watanabe H. Estimation of the dose of radiation received by patient and physician during a videofluoroscopic swallowing study. Dysphagia. 2016;31(4):574–8.CrossRefPubMed
37.
go back to reference Nuckolls AL, Worley C, Leto C, Zhang H, Morris JK, Stanford JA. Tongue force and tongue motility are differently affected by unilateral vs bilateral nigrostriatal dopamine depletion in rats. Behav Brain Res. 2012;234(2):343–8.CrossRefPubMedPubMedCentral Nuckolls AL, Worley C, Leto C, Zhang H, Morris JK, Stanford JA. Tongue force and tongue motility are differently affected by unilateral vs bilateral nigrostriatal dopamine depletion in rats. Behav Brain Res. 2012;234(2):343–8.CrossRefPubMedPubMedCentral
38.
go back to reference Park AM, Bhatt NK, Paniello RC. Paclitaxel inhibits post-traumatic recurrent laryngeal nerve regeneration into the posterior cricoarytenoid muscle in a canine model. Laryngoscope. 2016. doi:10.1002/lary.26058. Park AM, Bhatt NK, Paniello RC. Paclitaxel inhibits post-traumatic recurrent laryngeal nerve regeneration into the posterior cricoarytenoid muscle in a canine model. Laryngoscope. 2016. doi:10.​1002/​lary.​26058.
39.
go back to reference Pisegna JM, Kaneoka A, Pearson WG Jr, Kumar S, Langmore SE. Effects of non-invasive brain stimulation on post-stroke dysphagia: a systematic review and meta-analysis of randomized controlled trials. Clin Neurophysiol. 2016;127(1):956–68.CrossRefPubMed Pisegna JM, Kaneoka A, Pearson WG Jr, Kumar S, Langmore SE. Effects of non-invasive brain stimulation on post-stroke dysphagia: a systematic review and meta-analysis of randomized controlled trials. Clin Neurophysiol. 2016;127(1):956–68.CrossRefPubMed
40.
41.
go back to reference Ravosa MJ, Vinyard CJ, Gagnon M, Islam SA. Evolution of anthropoid jaw loading and kinematic patterns. Am J Phys Anthropol. 2000;112(4):493–516.CrossRefPubMed Ravosa MJ, Vinyard CJ, Gagnon M, Islam SA. Evolution of anthropoid jaw loading and kinematic patterns. Am J Phys Anthropol. 2000;112(4):493–516.CrossRefPubMed
42.
go back to reference Russell JA, Ciucci MR, Hammer MJ, Connor NP. Videofluorographic assessment of deglutitive behaviors in a rat model of aging and Parkinson disease. Dysphagia. 2013;28(1):95–104.CrossRefPubMed Russell JA, Ciucci MR, Hammer MJ, Connor NP. Videofluorographic assessment of deglutitive behaviors in a rat model of aging and Parkinson disease. Dysphagia. 2013;28(1):95–104.CrossRefPubMed
43.
go back to reference Satoh Y, Tsuji K, Tsujimura T, Ishizuka K, Inoue M. Suppression of the swallowing reflex by stimulation of the red nucleus. Brain Res Bull. 2015;116:25–33.CrossRefPubMed Satoh Y, Tsuji K, Tsujimura T, Ishizuka K, Inoue M. Suppression of the swallowing reflex by stimulation of the red nucleus. Brain Res Bull. 2015;116:25–33.CrossRefPubMed
44.
go back to reference Sugiyama N, Nishiyama E, Nishikawa Y, Sasamura T, Nakade S, Okawa K, Nagasawa T, Yuki A. A novel animal model of dysphagia following stroke. Dysphagia. 2014;29(1):61–7.CrossRefPubMed Sugiyama N, Nishiyama E, Nishikawa Y, Sasamura T, Nakade S, Okawa K, Nagasawa T, Yuki A. A novel animal model of dysphagia following stroke. Dysphagia. 2014;29(1):61–7.CrossRefPubMed
45.
go back to reference Thexton AJ, Crompton AW, German RZ. Electromyographic activity during the reflex pharyngeal swallow in the pig: Doty and Bosma (1956) revisited. J Appl Physiol. 2007;102(2):587–600.CrossRefPubMed Thexton AJ, Crompton AW, German RZ. Electromyographic activity during the reflex pharyngeal swallow in the pig: Doty and Bosma (1956) revisited. J Appl Physiol. 2007;102(2):587–600.CrossRefPubMed
46.
go back to reference Tsuji K, Tsujimura T, Magara J, Sakai S, Nakamura Y, Inoue M. Changes in the frequency of swallowing during electrical stimulation of superior laryngeal nerve in rats. Brain Res Bull. 2015;111:53–61.CrossRefPubMed Tsuji K, Tsujimura T, Magara J, Sakai S, Nakamura Y, Inoue M. Changes in the frequency of swallowing during electrical stimulation of superior laryngeal nerve in rats. Brain Res Bull. 2015;111:53–61.CrossRefPubMed
47.
go back to reference Tsujimura T, Tsuji K, Ariyasinghe S, Fukuhara T, Yamada A, Hayashi H, Nakamura Y, Iwata K, Inoue M. Differential involvement of two cortical masticatory areas in modulation of the swallowing reflex in rats. Neurosci Lett. 2012;528(2):159–64.CrossRefPubMed Tsujimura T, Tsuji K, Ariyasinghe S, Fukuhara T, Yamada A, Hayashi H, Nakamura Y, Iwata K, Inoue M. Differential involvement of two cortical masticatory areas in modulation of the swallowing reflex in rats. Neurosci Lett. 2012;528(2):159–64.CrossRefPubMed
48.
go back to reference Vinyard CJ, Williams SH, Wall CE, Johnson KR, Hylander WL. Jaw-muscle electromyography during chewing in Belanger’s treeshrews (Tupaia belangeri). Am J Phys Anthropol. 2005;127(1):26–45.CrossRefPubMed Vinyard CJ, Williams SH, Wall CE, Johnson KR, Hylander WL. Jaw-muscle electromyography during chewing in Belanger’s treeshrews (Tupaia belangeri). Am J Phys Anthropol. 2005;127(1):26–45.CrossRefPubMed
49.
go back to reference Vinyard CJ, Wall CE, Williams SH, Johnson KR, Hylander WL. Masseter electromyography during chewing in ring-tailed lemurs (Lemur catta). Am J Phys Anthropol. 2006;130(1):85–95.CrossRefPubMed Vinyard CJ, Wall CE, Williams SH, Johnson KR, Hylander WL. Masseter electromyography during chewing in ring-tailed lemurs (Lemur catta). Am J Phys Anthropol. 2006;130(1):85–95.CrossRefPubMed
50.
go back to reference Wall CE, Vinyard CJ, Johnson KR, Williams SH, Hylander WL. Phase II jaw movements and masseter muscle activity during chewing in Papio anubis. Am J Phys Anthropol. 2006;129(2):215–24.CrossRefPubMed Wall CE, Vinyard CJ, Johnson KR, Williams SH, Hylander WL. Phase II jaw movements and masseter muscle activity during chewing in Papio anubis. Am J Phys Anthropol. 2006;129(2):215–24.CrossRefPubMed
51.
go back to reference Walston J, Hadley EC, Ferrucci L, Guralnik JM, Newman AB, Studenski SA, Ershler WB, Harris T, Fried LP. Research agenda for frailty in older adults: toward a better understanding of physiology and etiology: summary from the American geriatrics society/National Institute on Aging Research Conference on frailty in older adults. J Am Geriatr Soc. 2006;54(6):991–1001.CrossRefPubMed Walston J, Hadley EC, Ferrucci L, Guralnik JM, Newman AB, Studenski SA, Ershler WB, Harris T, Fried LP. Research agenda for frailty in older adults: toward a better understanding of physiology and etiology: summary from the American geriatrics society/National Institute on Aging Research Conference on frailty in older adults. J Am Geriatr Soc. 2006;54(6):991–1001.CrossRefPubMed
52.
go back to reference Wirth R, et al. Oropharyngeal dysphagia in older persons—from pathophysiology to adequate intervention: a review and summary of an international expert meeting. Clin Interv Aging. 2016;11:189–208.CrossRefPubMedPubMedCentral Wirth R, et al. Oropharyngeal dysphagia in older persons—from pathophysiology to adequate intervention: a review and summary of an international expert meeting. Clin Interv Aging. 2016;11:189–208.CrossRefPubMedPubMedCentral
Metadata
Title
Animal Models for Dysphagia Studies: What Have We Learnt So Far
Authors
Rebecca Z. German
A. W. Crompton
Francois D. H. Gould
Allan J. Thexton
Publication date
01-02-2017
Publisher
Springer US
Published in
Dysphagia / Issue 1/2017
Print ISSN: 0179-051X
Electronic ISSN: 1432-0460
DOI
https://doi.org/10.1007/s00455-016-9778-7

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