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Sensory Stimulation Treatments for Oropharyngeal Dysphagia

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Dysphagia

Part of the book series: Medical Radiology ((Med Radiol Diagn Imaging))

Abstract

One of the main causes of dysphagia in older and neurological patients is the impairment on oropharyngeal sensory function. Over the last decade, a better understanding of how sensory stimuli are perceived in the human oropharynx and processed in the CNS has led to several new therapeutic strategies based on the sensory stimulation of the oropharynx in the treatment of dysphagia. The goal of these new strategies is not only to prevent safety impairments during deglutition but to improve the oropharyngeal swallow response to move from compensation to recovery of the swallowing function. This chapter will cover the neurophysiological, anatomical and molecular bases for these sensory stimulation treatments and provide an updated list of therapies that have been validated on patients with dysphagia, including pharmaceutical, physical and electrical stimulation of the oropharynx.

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References

  • Alessandri-Haber N, Yeh JJ, Boyd AE et al (2003) Hypotonicity induces TRPV4-mediated nociception in rat. Neuron 39:497–511

    Article  PubMed  CAS  Google Scholar 

  • Alessandri-Haber N, Dina OA, Chen X, Levine JD (2009) TRPC1 and TRPC6 channels cooperate with TRPV4 to mediate mechanical hyperalgesia and nociceptor sensitization. J Neurosci 29:6217–6228

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Alvarez-Berdugo D, Rofes L, Casamitjana JF et al (2016a) Oropharyngeal and laryngeal sensory innervation in the pathophysiology of swallowing disorders and sensory stimulation treatments. Ann N Y Acad Sci 1380:104–120

    Article  PubMed  Google Scholar 

  • Alvarez-Berdugo D, Rofes L, Farré R et al (2016b) Localization and expression of TRPV1 and TRPA1 in the human oropharynx and larynx. Neurogastroenterol Motil 28:91–100

    Article  PubMed  CAS  Google Scholar 

  • Alvarez-Berdugo D, Rofes L, Arreola V et al (2017) A comparative study on the therapeutic effect of TRPV1, TRPA1, and TRPM8 agonists on swallowing dysfunction associated with aging and neurological diseases. Neurogastroenterol Motil. https://doi.org/10.1111/nmo.13185. [Epub ahead of print]

  • Atoyan R, Shander D, Botchkareva NV (2009) Non-neuronal expression of transient receptor potential type A1 (TRPA1) in human skin. J Invest Dermatol 129:2312–2315

    Article  PubMed  CAS  Google Scholar 

  • Aviv JE, Martin JH, Jones ME et al (1994) Age-related changes in pharyngeal and supraglottic sensation. Ann Otol Rhinol Laryngol 103:749–752

    Article  PubMed  CAS  Google Scholar 

  • Aviv JE, Martin JH, Sacco RL et al (1996) Supraglottic and pharyngeal sensory abnormalities in stroke patients with dysphagia. Ann Otol Rhinol Laryngol 105:92–97

    Article  PubMed  CAS  Google Scholar 

  • Aviv JE, Sacco RL, Thomson J et al (1997) Silent laryngopharyngeal sensory deficits after stroke. Ann Otol Rhinol Laryngol 106:87–93

    Article  PubMed  CAS  Google Scholar 

  • Baijens LWJ, Speyer R, Passos VL et al (2013) Surface electrical stimulation in dysphagic Parkinson patients: a randomized clinical trial. Laryngoscope 123:38–44

    Article  Google Scholar 

  • Bandell M, Story GM, Hwang SW et al (2004) Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41:849–857

    Article  PubMed  CAS  Google Scholar 

  • Bautista DM, Movahed P, Hinman A et al (2005) Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci 102:12248–12252

    Article  PubMed  CAS  Google Scholar 

  • Beach TG, Adler CH, Sue LI et al (2010) Multi-organ distribution of phosphorylated alpha-synuclein histopathology in subjects with Lewy body disorders. Acta Neuropathol 119:689–702

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bengoechea GME, Alvarez Arenal A, Perez Casas A et al (1989) Microscopic innervation and nerve receptors of the lingual mucosa. Rev Eur Odontoestomatol 1:123–130

    Google Scholar 

  • Bonham AC, Sekizawa S, Chen C-Y, Joad JP (2006) Plasticity of brainstem mechanisms of cough. Respir Physiol Neurobiol 152:312–319

    Article  PubMed  Google Scholar 

  • Bülow M, Olsson R, Ekberg O (2003) Videoradiographic analysis of how carbonated thin liquids and thickened liquids affect the physiology of swallowing in subjects with aspiration on thin liquids. Acta Radiol 44:366–372

    Article  PubMed  Google Scholar 

  • Cabib C, Ortega O, Vilardell N, et al (2017) Chronic post-stroke oropharyngeal dysphagia is associated with impaired cortical activation to pharyngeal sensory inputs. Eur J Neurol 24:1355–1362

    Google Scholar 

  • Caterina MJ, Schumacher MA, Tominaga M et al (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816–824

    Article  PubMed  CAS  Google Scholar 

  • Caterina MJ, Rosen TA, Tominaga M et al (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398:436–441

    Article  PubMed  CAS  Google Scholar 

  • Chaudhari N, Roper SD (2010) The cell biology of taste. J Cell Biol 190:285–296

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chiba T, Watanabe S, Shin T (1985) Ultrastructure of the glomerular corpuscular nerve endings in the subepithelium of human epiglottis. Arch Histol Jpn 48:213–221

    Article  PubMed  CAS  Google Scholar 

  • Chouchkov CN (1973) On the fine structure of Krause’s bulbs in human skin, oral cavity and rectum. Arch Histol Jpn 35:365–375

    Article  PubMed  CAS  Google Scholar 

  • Chung MK, Lee H, Mizuno A et al (2004) TRPV3 and TRPV4 mediate warmth-evoked currents in primary mouse keratinocytes. J Biol Chem 279:21569–21575

    Article  PubMed  CAS  Google Scholar 

  • Clavé P, Shaker R (2015) Dysphagia: current reality and scope of the problem. Nat Rev Gastroenterol Hepatol 12:259–270

    Article  PubMed  Google Scholar 

  • Cola PC, Gatto AR, da Silva RG et al (2012) Taste and temperature in swallowing transit time after stroke. Cerebrovasc Dis Extra 2:45–51

    Article  PubMed  PubMed Central  Google Scholar 

  • Corey DP, García-Añoveros J, Holt JR et al (2004) TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432:723–730

    Article  PubMed  CAS  Google Scholar 

  • Cortright DN, Crandall M, Sanchez JF et al (2001) The tissue distribution and functional characterization of human VR1. Biochem Biophys Res Commun 281:1183–1189

    Article  PubMed  CAS  Google Scholar 

  • Delany NS, Hurle M, Facer P et al (2001) Identification and characterization of a novel human vanilloid receptor-like protein, VRL-2. Physiol Genomics 4:165–174

    Article  PubMed  CAS  Google Scholar 

  • Denda M, Fuziwara S, Inoue K et al (2001) Immunoreactivity of VR1 on epidermal keratinocyte of human skin. Biochem Biophys Res Commun 285:1250–1252

    Article  PubMed  CAS  Google Scholar 

  • Dziewas R, Mistry S, Hamdy S et al (2017) Design and implementation of pharyngeal electrical stimulation for early de-cannulation in TRACheotomized (PHAST-TRAC) stroke patients with neurogenic dysphagia: a prospective randomized single-blinded interventional study. Int J Stroke 12:430–437

    Article  PubMed  Google Scholar 

  • Ebihara T, Sekizawa K, Nakazawa H, Sasaki H (1993) Capsaicin and swallowing reflex. Lancet (London, England) 341:432

    Article  CAS  Google Scholar 

  • Ebihara T, Takahashi H, Ebihara S et al (2005) Capsaicin troche for swallowing dysfunction in older people. J Am Geriatr Soc 53:824–828

    Article  PubMed  Google Scholar 

  • Ebihara T, Ebihara S, Maruyama M et al (2006a) A randomized trial of olfactory stimulation using black pepper oil in older people with swallowing dysfunction. J Am Geriatr Soc 54:1401–1406

    Article  PubMed  Google Scholar 

  • Ebihara T, Ebihara S, Watando A et al (2006b) Effects of menthol on the triggering of the swallowing reflex in elderly patients with dysphagia. Br J Clin Pharmacol 62:369–371

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ebihara T, Ebihara S, Yamazaki M et al (2010) Intensive stepwise method for oral intake using a combination of transient receptor potential stimulation and olfactory stimulation inhibits the incidence of pneumonia in dysphagic older adults. J Am Geriatr Soc 58:196–198

    Article  PubMed  Google Scholar 

  • Elshukri O, Michou E, Mentz H, Hamdy S (2016) Brain and behavioral effects of swallowing carbonated water on the human pharyngeal motor system. J Appl Physiol 120:408–415

    Article  PubMed  CAS  Google Scholar 

  • Fraser C, Power M, Hamdy S et al (2002) Driving plasticity in human adult motor cortex is associated with improved motor function after brain injury. Neuron 34:831–840

    Article  PubMed  CAS  Google Scholar 

  • Freed ML, Freed L, Chatburn RL, Christian M (2001) Electrical stimulation for swallowing disorders caused by stroke. Respir Care 46:466–474

    PubMed  CAS  Google Scholar 

  • Gallas S, Marie JP, Leroi AM, Verin E (2010) Sensory transcutaneous electrical stimulation improves post-stroke dysphagic patients. Dysphagia 25:291–297

    Article  PubMed  Google Scholar 

  • García-Añoveros J, Duggan A (2007) TRPA1 in auditory and nociceptive organs. In: Liedtke WB, Heller S (eds) TRP ion channel function in sensory transduction and cellular signaling cascades. CRC Press/Taylor & Francis, Boca Raton

    Google Scholar 

  • Geppetti P, Trevisani M (2004) Activation and sensitisation of the vanilloid receptor: role in gastrointestinal inflammation and function. Br J Pharmacol 141:1313–1320

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hamdy S, Aziz Q, Rothwell JC et al (1996) The cortical topography of human swallowing musculature in health and disease. Nat Med 2:1217–1224

    Article  PubMed  CAS  Google Scholar 

  • Hamdy S, Aziz Q, Rothwell JC et al (1997) Explaining oropharyngeal dysphagia after unilateral hemispheric stroke. Lancet 350:686–692

    Article  PubMed  CAS  Google Scholar 

  • Hamdy S, Jilani S, Price V et al (2003) Modulation of human swallowing behaviour by thermal and chemical stimulation in health and after brain injury. Neurogastroenterol Motil 15:69–77

    Article  PubMed  CAS  Google Scholar 

  • Hammer MJ, Murphy CA, Abrams TM (2013) Airway somatosensory deficits and dysphagia in Parkinson’s disease. J Parkinsons Dis 3:39–44

    PubMed  PubMed Central  Google Scholar 

  • Hashimoto K (1972) Fine structure of Merkel cell in human oral mucosa. J Invest Dermatol 58:381–387

    Article  PubMed  CAS  Google Scholar 

  • Huque T, Cowart BJ, Dankulich-Nagrudny L et al (2009) Sour ageusia in two individuals implicates ion channels of the ASIC and PKD families in human sour taste perception at the anterior tongue. PLoS One 4:e7347

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jayasekeran V, Singh S, Tyrrell P et al (2010) Adjunctive functional pharyngeal electrical stimulation reverses swallowing disability after brain lesions. Gastroenterology 138:1737–1746.e2

    Article  PubMed  Google Scholar 

  • Jean A (2001) Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev 81:929–969

    Article  PubMed  CAS  Google Scholar 

  • Karashima Y, Damann N, Prenen J et al (2007) Bimodal action of menthol on the transient receptor potential channel TRPA1. J Neurosci 27:9874–9884

    Article  PubMed  CAS  Google Scholar 

  • Kedei N, Szabo T, Lile JD et al (2001) Analysis of the native quaternary structure of vanilloid receptor 1. J Biol Chem 276:28613–28619

    Article  PubMed  CAS  Google Scholar 

  • Kitagawa J-I, Shingai T, Takahashi Y et al (2002) Pharyngeal branch of the glossopharyngeal nerve plays a major role in reflex swallowing from the pharynx. Am J Physiol Regul Integr Comp Physiol 282:R1342–R1347

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi K, Fukuoka T, Obata K et al (2005) Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with Aδ/C-fibers and colocalization with Trk receptors. J Comp Neurol 493:596–606

    Article  PubMed  CAS  Google Scholar 

  • de Lama Lazzara G, Lazarus C, Logemann JA (1986) Impact of thermal stimulation on the triggering of the swallowing reflex. Dysphagia 1:73–77

    Article  Google Scholar 

  • Larsson V, Torisson G, Bülow M, Londos E (2017) Effects of carbonated liquid on swallowing dysfunction in dementia with Lewy bodies and Parkinson’s disease dementia. Clin Interv Aging 12:1215–1222

    Article  PubMed  PubMed Central  Google Scholar 

  • Lawrenson JG, Ruskell GL (1991) The structure of corpuscular nerve endings in the limbal conjunctiva of the human eye. J Anat 177:75–84

    PubMed  PubMed Central  CAS  Google Scholar 

  • Leffler A, Mönter B, Koltzenburg M (2006) The role of the capsaicin receptor TRPV1 and acid-sensing ion channels (ASICS) in proton sensitivity of subpopulations of primary nociceptive neurons in rats and mice. Neuroscience 139:699–709

    Article  PubMed  CAS  Google Scholar 

  • Logemann JA (2007) The effects of VitalStim on clinical and research thinking in dysphagia. Dysphagia 22:11–12

    Article  PubMed  Google Scholar 

  • Logemann JA, Pauloski BR, Colangelo L et al (1995) Effects of a sour bolus on oropharyngeal swallowing measures in patients with neurogenic dysphagia. J Speech Hear Res 38:556–563

    Article  PubMed  CAS  Google Scholar 

  • Ludlow CL, Humbert I, Saxon K et al (2007) Effects of surface electrical stimulation both at rest and during swallowing in chronic pharyngeal dysphagia. Dysphagia 22:1–10

    Article  PubMed  PubMed Central  Google Scholar 

  • Mortelliti AJ, Malmgren LT, Gacek RR (1990) Ultrastructural changes with age in the human superior laryngeal nerve. Arch Otolaryngol Head Neck Surg 116:1062–1069

    Article  PubMed  CAS  Google Scholar 

  • Mosavi LK, Minor DL, Peng Z-Y (2002) Consensus-derived structural determinants of the ankyrin repeat motif. Proc Natl Acad Sci 99:16029–16034

    Article  PubMed  CAS  Google Scholar 

  • Mu L, Sanders I (2000) Sensory nerve supply of the human oro- and laryngopharynx: a preliminary study. Anat Rec 258:406–420

    Article  PubMed  CAS  Google Scholar 

  • Mu L, Sobotka S, Chen J et al (2013) Parkinson disease affects peripheral sensory nerves in the pharynx. J Neuropathol Exp Neurol 72:614–623

    Article  PubMed  PubMed Central  Google Scholar 

  • Mu L, Chen J, Sobotka S et al (2015) Alpha-synuclein pathology in sensory nerve terminals of the upper aerodigestive tract of Parkinson’s disease patients. Dysphagia 30:404–417

    Article  PubMed  PubMed Central  Google Scholar 

  • Mukhopadhyay I, Gomes P, Aranake S et al (2011) Expression of functional TRPA1 receptor on human lung fibroblast and epithelial cells. J Recept Signal Transduct Res 31:350–358

    Article  PubMed  CAS  Google Scholar 

  • Munger BL (1965) The intraepidermal innervation of the snout skin of the opossum. A light and electron microscope study, with observations on the nature of Merkel’s Tastzellen. J Cell Biol 26:79–97

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Munger BL, Ide C (1988) The structure and function of cutaneous sensory receptors. Arch Histol Cytol 51:1–34

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa T, Takashi Ohrui KS, Sasaki H (1995) Sputum substance P in aspiration pneumonia. Lancet 345:1447

    Article  PubMed  CAS  Google Scholar 

  • Nakato R, Manabe N, Shimizu S et al (2017) Effects of capsaicin on older patients with oropharyngeal dysphagia: a double-blind, placebo-controlled, crossover study. Digestion 95:210–220

    Article  PubMed  CAS  Google Scholar 

  • Nilius B, Owsianik G, Voets T, Peters JA (2007) Transient receptor potential cation channels in disease. Physiol Rev 87:165–217

    Article  PubMed  CAS  Google Scholar 

  • Oh BM, Kim DY, Paik NJ (2007) Recovery of swallowing function is accompanied by the expansion of the cortical map. Int J Neurosci 117:1215–1227

    Article  PubMed  Google Scholar 

  • Okubo T, Clark C, Hogan BLM (2009) Cell lineage mapping of taste bud cells and keratinocytes in the mouse tongue and soft palate. Stem Cells 27:442–450

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ortega O, Rofes L, Martin A et al (2016) A comparative study between two sensory stimulation strategies after two weeks treatment on older patients with oropharyngeal dysphagia. Dysphagia 31:706–716

    Article  PubMed  Google Scholar 

  • Page AJ, Brierley SM, Martin CM et al (2005) Different contributions of ASIC channels 1a, 2, and 3 in gastrointestinal mechanosensory function. Gut 54:1408–1415

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Peier AM (2002) A heat-sensitive TRP channel expressed in keratinocytes. Science 296:2046–2049

    Article  PubMed  CAS  Google Scholar 

  • Peier AM, Moqrich A, Hergarden AC et al (2002) A TRP channel that senses cold stimuli and menthol. Cell 108:705–715

    Article  PubMed  CAS  Google Scholar 

  • Pelletier CA, Lawless HT (2003) Effect of citric acid and citric acid-sucrose mixtures on swallowing in neurogenic oropharyngeal dysphagia. Dysphagia 18:231–241

    Article  PubMed  Google Scholar 

  • Phelps CB, Gaudet R (2007) The role of the N terminus and transmembrane domain of TRPM8 in channel localization and tetramerization. J Biol Chem 282:36474–36480

    Article  PubMed  CAS  Google Scholar 

  • Pommerenke WT (1927) A study of the sensory areas eliciting the swallowing reflexes. Am J Physiol 84:36–41

    Google Scholar 

  • Purves D, Augustine GJ, Fitzpatrick D et al (eds) (2012) Neuroscience, 5th edn. Sunderland, Sinauer Associates Inc.

    Google Scholar 

  • Rathee PK, Distler C, Obreja O et al (2002) PKA/AKAP/VR-1 module: a common link of Gs-mediated signaling to thermal hyperalgesia. J Neurosci 22:4740–4745

    Article  PubMed  CAS  Google Scholar 

  • Regan J, Walshe M, Tobin WO (2010) Immediate effects of thermal-tactile stimulation on timing of swallow in idiopathic Parkinson’s disease. Dysphagia 25:207–215

    Article  PubMed  Google Scholar 

  • Rofes L, Arreola V, López I et al (2013a) Effect of surface sensory and motor electrical stimulation on chronic poststroke oropharyngeal dysfunction. Neurogastroenterol Motil 25:888–896

    Article  PubMed  CAS  Google Scholar 

  • Rofes L, Arreola V, Martin A, Clavé P (2013b) Natural capsaicinoids improve swallow response in older patients with oropharyngeal dysphagia. Gut 62:1280–1287

    Article  PubMed  Google Scholar 

  • Rofes L, Arreola V, Martin A, Clavé P (2014a) Effect of oral piperine on the swallow response of patients with oropharyngeal dysphagia. J Gastroenterol 49:1517–1523

    Article  PubMed  Google Scholar 

  • Rofes L, Cola P, Clavé P (2014b) The effects of sensory stimulation on neurogenic oropharyngeal dysphagia. J Gastroenterol Hepatol Res 3:1066–1072

    Google Scholar 

  • Rofes L, Ortega O, Vilardell N et al (2017) Spatiotemporal characteristics of the pharyngeal event-related potential in healthy subjects and older patients with oropharyngeal dysfunction. Neurogastroenterol Motil 29(2)

    Google Scholar 

  • Roper SD (1989) The cell biology of vertebrate taste receptors. Annu Rev Neurosci 12:329–353

    Article  PubMed  CAS  Google Scholar 

  • Rosenbaum T, Simon SA (2007) TRPV1 receptors and signal transduction. In: Liedtke WB, Heller S (eds) TRP ion channel function in sensory transduction and cellular signaling cascades. CRC Press/Taylor & Francis, Boca Raton

    Google Scholar 

  • Rosenbaum T, Gordon-Shaag A, Munari M, Gordon SE (2004) Ca 2+/calmodulin modulates TRPV1 activation by capsaicin. J Gen Physiol 123:53–62

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanders I, Mu L (1998) Anatomy of the human internal superior laryngeal nerve. Anat Rec 252:646–656

    Article  PubMed  CAS  Google Scholar 

  • Sasaki R, Sato T, Yajima T et al (2013) The distribution of TRPV1 and TRPV2 in the rat pharynx. Cell Mol Neurobiol 33:707–714

    Article  PubMed  CAS  Google Scholar 

  • Schindler JS, Kelly JH (2002) Swallowing disorders in the elderly. Laryngoscope 112:589–602

    Article  PubMed  Google Scholar 

  • Scutt P, Lee HS, Hamdy S, Bath PM (2015) Pharyngeal electrical stimulation for treatment of Poststroke dysphagia: individual patient data meta-analysis of randomised controlled trials. Stroke Res Treat 2015:1–8

    Article  Google Scholar 

  • Sdravou K, Walshe M, Dagdilelis L (2012) Effects of carbonated liquids on oropharyngeal swallowing measures in people with neurogenic dysphagia. Dysphagia 27:240–250

    Article  PubMed  Google Scholar 

  • Shabir S, Cross W, Kirkwood LA et al (2013) Functional expression of purinergic P2 receptors and transient receptor potential channels by the human urothelium. Am J Physiol Renal Physiol 305:F396–F406

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Singh S, Hamdy S (2006) Dysphagia in stroke patients. Postgrad Med J 82:383–391

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smith KR (1970) The ultrastructure of the human Haarscheibe and Merkel cell. J Invest Dermatol 54:150–159

    Article  PubMed  Google Scholar 

  • Sotomayor M, Corey DP, Schulten K (2005) In search of the hair-cell gating spring: elastic properties of ankyrin and cadherin repeats. Structure 13:669–682

    Article  PubMed  CAS  Google Scholar 

  • Stone LM, Finger TE, Tam PP, Tan SS (1995) Taste receptor cells arise from local epithelium, not neurogenic ectoderm. Proc Natl Acad Sci U S A 92:1916–1920

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Story GM, Peier AM, Reeve AJ et al (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819–829

    Article  PubMed  CAS  Google Scholar 

  • Suntrup S, Marian T, Schröder JB et al (2015) Electrical pharyngeal stimulation for dysphagia treatment in tracheotomized stroke patients: a randomized controlled trial. Intensive Care Med 41:1629–1637

    Article  PubMed  CAS  Google Scholar 

  • Suntrup-Krueger S, Bittner S, Recker S et al (2016) Electrical pharyngeal stimulation increases substance P level in saliva. Neurogastroenterol Motil 28:855–860

    Article  PubMed  CAS  Google Scholar 

  • Szallasi A, Cortright DN, Blum CA, Eid SR (2007) The vanilloid receptor TRPV1: 10 years from channel cloning to antagonist proof-of-concept. Nat Rev Drug Discov 6:357–372

    Article  PubMed  CAS  Google Scholar 

  • Teismann IK, Steinsträter O, Warnecke T et al (2009) Tactile thermal oral stimulation increases the cortical representation of swallowing. BMC Neurosci 10:71

    Article  PubMed  PubMed Central  Google Scholar 

  • Teismann IK, Suntrup S, Warnecke T et al (2011) Cortical swallowing processing in early subacute stroke. BMC Neurol 11:34

    Article  PubMed  PubMed Central  Google Scholar 

  • Theurer JA, Johnston JL, Fisher J et al (2013) Proof-of-principle pilot study of oropharyngeal air-pulse application in individuals with dysphagia after hemispheric stroke. Arch Phys Med Rehabil 94:1088–1094

    Article  PubMed  Google Scholar 

  • Tiago R, Pontes P, do Brasil OC (2007) Age-related changes in human laryngeal nerves. Otolaryngol Neck Surg 136:747–751

    Article  Google Scholar 

  • Tomchik SM, Berg S, Kim JW et al (2007) Breadth of tuning and taste coding in mammalian taste buds. J Neurosci 27:10840–10848

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Toyoshima K, Miyamoto K, Itoh A, Shimamura A (1987) Merkel-neurite complexes in the fungiform papillae of two species of monkeys. Cell Tissue Res 250:237–239

    Article  PubMed  CAS  Google Scholar 

  • Ugawa S, Ueda T, Yamamura H et al (2005) Coexpression of vanilloid receptor subtype-1 and acid-sensing ion channel genes in the human trigeminal ganglion neurons. Chem Senses 30(Suppl 1):270287

    Google Scholar 

  • Vandenbeuch A, Clapp TR, Kinnamon SC (2008) Amiloride-sensitive channels in type I fungiform taste cells in mouse. BMC Neurosci 9:1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Voets T (2014) TRP channels and thermosensation. In: Handbook of experimental pharmacology. Springer, Berlin, pp 729–741

    Google Scholar 

  • Watanabe I (1982) Fine structure of lamellated nerve endings in the gingiva of man and the Cebus apella monkey. Okajimas Folia Anat Jpn 59:181–198

    Article  PubMed  CAS  Google Scholar 

  • Watanabe I (2004) Ultrastructures of mechanoreceptors in the oral mucosa. Anat Sci Int 79:55–61

    Article  PubMed  Google Scholar 

  • Watanabe I, Yamada E (1983) The fine structure of lamellated nerve endings found in the rat gingiva. Arch Histol Jpn 46:173–182

    Article  PubMed  CAS  Google Scholar 

  • Watanabe I, Yamada E (1985) A light and electron microscopic study of lamellated nerve endings found in the rat cheek mucosa. Arch Histol Jpn 48:497–504

    Article  PubMed  CAS  Google Scholar 

  • Witt M, Reutter K (1997) Scanning electron microscopical studies of developing gustatory papillae in humans. Chem Senses 22:601–612

    Article  PubMed  CAS  Google Scholar 

  • Xu H, Ramsey IS, Kotecha SA (2002) TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418:181–186

    Article  PubMed  CAS  Google Scholar 

  • Xu H, Delling M, Jun JC, Clapham DE (2006) Oregano, thyme and clove-derived flavors and skin sensitizers activate specific TRP channels. Nat Neurosci 9:628–635

    Article  PubMed  CAS  Google Scholar 

  • Yatake Y, Hiroto I (1968) Anatomical study on the laryngeal nerves of mammals. Nihon Jibiinkoka Gakkai Kaiho 71:212–216

    Article  PubMed  Google Scholar 

  • Yee NS (2015) Roles of TRPM8 ion channels in cancer: proliferation, survival, and invasion. Cancers (Basel) 7:2134–2146

    Article  CAS  Google Scholar 

  • Yee CL, Yang R, Böttger B et al (2001) “Type III” cells of rat taste buds: immunohistochemical and ultrastructural studies of neuron-specific enolase, protein gene product 9.5, and serotonin. J Comp Neurol 440:97–108

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Hoon MA, Chandrashekar J et al (2003) Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112:293–301

    Article  PubMed  CAS  Google Scholar 

  • Zur KB, Mu L, Sanders I (2004) Distribution pattern of the human lingual nerve. Clin Anat 17:88–92

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Gastrointestinal Tract Motility Laboratory, CIBERehd-CSdM, Hospital de Mataró, Mataró, Spain

    Daniel Alvarez-Berdugo, Noemí Tomsen & Pere Clavé

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  1. Daniel Alvarez-Berdugo
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  3. Pere Clavé
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Correspondence to Pere Clavé .

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  1. Department of Translational Medicine, Lund University, Department of Medical Imaging and Physiology, Skåne University Hospital, Malmö, Sweden

    Olle Ekberg

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Alvarez-Berdugo, D., Tomsen, N., Clavé, P. (2018). Sensory Stimulation Treatments for Oropharyngeal Dysphagia. In: Ekberg, O. (eds) Dysphagia. Medical Radiology(). Springer, Cham. https://doi.org/10.1007/174_2017_166

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  • DOI: https://doi.org/10.1007/174_2017_166

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  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-68571-7

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