Skip to main content
Top
Published in: Journal of Gastroenterology 12/2014

01-12-2014 | Original Article—Alimentary Tract

Effect of oral piperine on the swallow response of patients with oropharyngeal dysphagia

Authors: Laia Rofes, Viridiana Arreola, Alberto Martin, Pere Clavé

Published in: Journal of Gastroenterology | Issue 12/2014

Login to get access

Abstract

Background

Oropharyngeal dysphagia (OD) is a major gastrointestinal motility disorder that causes severe nutritional and respiratory complications in elderly and neurological patients. In an earlier study, we found that stimulation of pharyngeal sensory neurons by capsaicinoids acting on transient receptor potential vanilloid 1 (TRPV1) improved the swallow response of dysphagic patients. The aim of this study was to explore the effect of piperine, a dual TRPV1/TRPA1 agonist, on the swallow response of dysphagic patients.

Methods

A videofluoroscopic study was performed to assess the signs of impaired safety and efficacy of swallow and the swallow response of 40 dysphagic patients while swallowing one series of nectar control boluses and two series of nectar boluses supplemented with piperine. Patients were randomized into two groups: one group received 150 μM piperine and the other group received 1 mM.

Results

Piperine improved the safety of swallow by: (a) reducing the prevalence of unsafe swallows by −34.48 % (P = 0.004) at 150 μM and −57.19 % (P < 0.001) at 1 mM, and the severity score of the penetration-aspiration scale from 3.25 ± 0.51 to 1.85 ± 0.27 (P = 0.003, 1 mM); and (b) shortening the time to laryngeal vestibule closure from 0.366 ± 0.024 to 0.270 ± 0.022 s with 150 μM piperine (P < 0.001) and from 0.380 ± 0.032 to 0.306 ± 0.028 s with 1 mM piperine (P < 0.05).

Conclusions

Supplementing the alimentary bolus with piperine speeds swallow response and strongly improves safety of swallow in patients with OD, with a maximal therapeutic effect at 1 mM. Our results suggest that activation of TRPV1/A1 in oropharyngeal sensory neurons is a very promising neurostimulation strategy for dysphagic patients.
Literature
2.
go back to reference Serra-Prat M, Hinojosa G, Lopez D, et al. Prevalence of oropharyngeal dysphagia and impaired safety and efficacy of swallow in independently living older persons. J Am Geriatr Soc. 2011;59:186–7.PubMedCrossRef Serra-Prat M, Hinojosa G, Lopez D, et al. Prevalence of oropharyngeal dysphagia and impaired safety and efficacy of swallow in independently living older persons. J Am Geriatr Soc. 2011;59:186–7.PubMedCrossRef
3.
go back to reference Lin LC, Wu SC, Chen HS, Wang TG, Chen MY. Prevalence of impaired swallowing in institutionalized older people in Taiwan. J Am Geriatr Soc. 2002;50:1118–23.PubMedCrossRef Lin LC, Wu SC, Chen HS, Wang TG, Chen MY. Prevalence of impaired swallowing in institutionalized older people in Taiwan. J Am Geriatr Soc. 2002;50:1118–23.PubMedCrossRef
4.
go back to reference Martino R, Foley N, Bhogal S, Diamant N, Speechley M, Teasell R. Dysphagia after stroke: incidence, diagnosis, and pulmonary complications. Stroke. 2005;36:2756–63.PubMedCrossRef Martino R, Foley N, Bhogal S, Diamant N, Speechley M, Teasell R. Dysphagia after stroke: incidence, diagnosis, and pulmonary complications. Stroke. 2005;36:2756–63.PubMedCrossRef
5.
go back to reference Kalf JG, de Swart BJM, Bloem BR, Munneke M. Prevalence of oropharyngeal dysphagia in Parkinson’s disease: a meta-analysis. Parkinsonism Relat Disord. 2012;18:311–5.PubMedCrossRef Kalf JG, de Swart BJM, Bloem BR, Munneke M. Prevalence of oropharyngeal dysphagia in Parkinson’s disease: a meta-analysis. Parkinsonism Relat Disord. 2012;18:311–5.PubMedCrossRef
6.
go back to reference Prosiegel M, Schelling A, Wagner-Sonntag E. Dysphagia and multiple sclerosis. Int MS J. 2004;11:22–31.PubMed Prosiegel M, Schelling A, Wagner-Sonntag E. Dysphagia and multiple sclerosis. Int MS J. 2004;11:22–31.PubMed
7.
go back to reference Clave P, de Kraa M, Arreola V, et al. The effect of bolus viscosity on swallowing function in neurogenic dysphagia. Aliment Pharmacol Ther. 2006;24:1385–94.PubMedCrossRef Clave P, de Kraa M, Arreola V, et al. The effect of bolus viscosity on swallowing function in neurogenic dysphagia. Aliment Pharmacol Ther. 2006;24:1385–94.PubMedCrossRef
8.
go back to reference Rofes L, Arreola V, Romea M, et al. Pathophysiology of oropharyngeal dysphagia in the frail elderly. Neurogastroenterol Motil. 2010;22(851–8):e230. Rofes L, Arreola V, Romea M, et al. Pathophysiology of oropharyngeal dysphagia in the frail elderly. Neurogastroenterol Motil. 2010;22(851–8):e230.
9.
go back to reference Aviv JE, Martin JH, Jones ME, et al. Age-related changes in pharyngeal and supraglottic sensation. Ann Otol Rhinol Laryngol. 1994;103:749–52.PubMedCrossRef Aviv JE, Martin JH, Jones ME, et al. Age-related changes in pharyngeal and supraglottic sensation. Ann Otol Rhinol Laryngol. 1994;103:749–52.PubMedCrossRef
10.
go back to reference Aviv JE, Martin JH, Sacco RL, et al. Supraglottic and pharyngeal sensory abnormalities in stroke patients with dysphagia. Ann Otol Rhinol Laryngol. 1996;105:92–7.PubMedCrossRef Aviv JE, Martin JH, Sacco RL, et al. Supraglottic and pharyngeal sensory abnormalities in stroke patients with dysphagia. Ann Otol Rhinol Laryngol. 1996;105:92–7.PubMedCrossRef
12.
go back to reference Speyer R, Baijens L, Heijnen M, Zwijnenberg I. Effects of therapy in oropharyngeal dysphagia by speech and language therapists: a systematic review. Dysphagia. 2010;25:40–65.PubMedCentralPubMedCrossRef Speyer R, Baijens L, Heijnen M, Zwijnenberg I. Effects of therapy in oropharyngeal dysphagia by speech and language therapists: a systematic review. Dysphagia. 2010;25:40–65.PubMedCentralPubMedCrossRef
13.
go back to reference Rofes L, Arreola V, Martin A, Clavé P. Natural capsaicinoids improve swallow response in older patients with oropharyngeal dysphagia. Gut. 2013;62:1280–7.PubMedCrossRef Rofes L, Arreola V, Martin A, Clavé P. Natural capsaicinoids improve swallow response in older patients with oropharyngeal dysphagia. Gut. 2013;62:1280–7.PubMedCrossRef
14.
go back to reference Ebihara T, Ebihara S, Maruyama M, et al. A randomized trial of olfactory stimulation using black pepper oil in older people with swallowing dysfunction. J Am Geriatr Soc. 2006;54:1401–6.PubMedCrossRef Ebihara T, Ebihara S, Maruyama M, et al. A randomized trial of olfactory stimulation using black pepper oil in older people with swallowing dysfunction. J Am Geriatr Soc. 2006;54:1401–6.PubMedCrossRef
15.
go back to reference Hamdy S, Jilani S, Price V, Parker C, Hall N, Power M. Modulation of human swallowing behaviour by thermal and chemical stimulation in health and after brain injury. Neurogastroenterol Motil. 2003;15:69–77.PubMedCrossRef Hamdy S, Jilani S, Price V, Parker C, Hall N, Power M. Modulation of human swallowing behaviour by thermal and chemical stimulation in health and after brain injury. Neurogastroenterol Motil. 2003;15:69–77.PubMedCrossRef
16.
go back to reference Logemann JA, Pauloski BR, Colangelo L, Lazarus C, Fujiu M, Kahrilas PJ. Effects of a sour bolus on oropharyngeal swallowing measures in patients with neurogenic dysphagia. J Speech Hear Res. 1995;38:556–63.PubMedCrossRef Logemann JA, Pauloski BR, Colangelo L, Lazarus C, Fujiu M, Kahrilas PJ. Effects of a sour bolus on oropharyngeal swallowing measures in patients with neurogenic dysphagia. J Speech Hear Res. 1995;38:556–63.PubMedCrossRef
17.
go back to reference Ebihara T, Ebihara S, Watando A, et al. Effects of menthol on the triggering of the swallowing reflex in elderly patients with dysphagia. Br J Clin Pharmacol. 2006;62:369–71.PubMedCentralPubMedCrossRef Ebihara T, Ebihara S, Watando A, et al. Effects of menthol on the triggering of the swallowing reflex in elderly patients with dysphagia. Br J Clin Pharmacol. 2006;62:369–71.PubMedCentralPubMedCrossRef
18.
go back to reference Watando A, Ebihara S, Ebihara T, et al. Effect of temperature on swallowing reflex in elderly patients with aspiration pneumonia. J Am Geriatr Soc. 2004;52:2143–4.PubMedCrossRef Watando A, Ebihara S, Ebihara T, et al. Effect of temperature on swallowing reflex in elderly patients with aspiration pneumonia. J Am Geriatr Soc. 2004;52:2143–4.PubMedCrossRef
19.
go back to reference Okumura Y, Narukawa M, Iwasaki Y, et al. Activation of TRPV1 and TRPA1 by black pepper components. Biosci Biotechnol Biochem. 2010;74:1068–72.PubMedCrossRef Okumura Y, Narukawa M, Iwasaki Y, et al. Activation of TRPV1 and TRPA1 by black pepper components. Biosci Biotechnol Biochem. 2010;74:1068–72.PubMedCrossRef
20.
go back to reference Clave 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.PubMedCrossRef Clave 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.PubMedCrossRef
21.
go back to reference Vellas B, Guigoz Y, Garry PJ, et al. The mini nutritional assessment (MNA) and its use in grading the nutritional state of elderly patients. Nutrition. 1999;15:116–22.PubMedCrossRef Vellas B, Guigoz Y, Garry PJ, et al. The mini nutritional assessment (MNA) and its use in grading the nutritional state of elderly patients. Nutrition. 1999;15:116–22.PubMedCrossRef
22.
go back to reference Belafsky PC, Mouadeb DA, Rees CJ, et al. Validity and reliability of the eating assessment tool (EAT-10). Ann Otol Rhinol Laryngol. 2008;117:919–24.PubMedCrossRef Belafsky PC, Mouadeb DA, Rees CJ, et al. Validity and reliability of the eating assessment tool (EAT-10). Ann Otol Rhinol Laryngol. 2008;117:919–24.PubMedCrossRef
23.
go back to reference Wallace KL, Middleton S, Cook IJ. Development and validation of a self-report symptom inventory to assess the severity of oral-pharyngeal dysphagia. Gastroenterology. 2000;118:678–87.PubMedCrossRef Wallace KL, Middleton S, Cook IJ. Development and validation of a self-report symptom inventory to assess the severity of oral-pharyngeal dysphagia. Gastroenterology. 2000;118:678–87.PubMedCrossRef
24.
25.
go back to reference Rofes L, Vilardell N, Clave P. Post-stroke dysphagia: progress at last. Neurogastroenterol Motil. 2013;25:278–82.PubMedCrossRef Rofes L, Vilardell N, Clave P. Post-stroke dysphagia: progress at last. Neurogastroenterol Motil. 2013;25:278–82.PubMedCrossRef
26.
go back to reference Teismann IK, Steinstrater O, Warnecke T, et al. Tactile thermal oral stimulation increases the cortical representation of swallowing. BMC Neurosci. 2009;10:71.PubMedCentralPubMedCrossRef Teismann IK, Steinstrater O, Warnecke T, et al. Tactile thermal oral stimulation increases the cortical representation of swallowing. BMC Neurosci. 2009;10:71.PubMedCentralPubMedCrossRef
27.
go back to reference Gallas S, Marie JP, Leroi AM, Verin E. Sensory transcutaneous electrical stimulation improves post-stroke dysphagic patients. Dysphagia. 2010;25:291–7.PubMedCrossRef Gallas S, Marie JP, Leroi AM, Verin E. Sensory transcutaneous electrical stimulation improves post-stroke dysphagic patients. Dysphagia. 2010;25:291–7.PubMedCrossRef
28.
go back to reference Jayasekeran V, Singh S, Tyrrell P, et al. Adjunctive functional pharyngeal electrical stimulation reverses swallowing disability after brain lesions. Gastroenterology. 2010;138:1737–46.PubMedCrossRef Jayasekeran V, Singh S, Tyrrell P, et al. Adjunctive functional pharyngeal electrical stimulation reverses swallowing disability after brain lesions. Gastroenterology. 2010;138:1737–46.PubMedCrossRef
29.
go back to reference Park JW, Oh JC, Lee JW, Yeo JS, Ryu KH. The effect of 5 Hz high-frequency rTMS over contralesional pharyngeal motor cortex in post-stroke oropharyngeal dysphagia: a randomized controlled study. Neurogastroenterol Motil. 2013;25:324-e250.PubMed Park JW, Oh JC, Lee JW, Yeo JS, Ryu KH. The effect of 5 Hz high-frequency rTMS over contralesional pharyngeal motor cortex in post-stroke oropharyngeal dysphagia: a randomized controlled study. Neurogastroenterol Motil. 2013;25:324-e250.PubMed
30.
31.
go back to reference Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81:929–69.PubMed Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81:929–69.PubMed
32.
go back to reference Nakashimo Y, Takumida M, Fukuiri T, Anniko M, Hirakawa K. Expression of transient receptor potential channel vanilloid (TRPV) 1–4, melastin (TRPM) 5 and 8, and ankyrin (TRPA1) in the normal and methimazole-treated mouse olfactory epithelium. Acta Otolaryngol. 2010;130:1278–86.PubMedCentralPubMedCrossRef Nakashimo Y, Takumida M, Fukuiri T, Anniko M, Hirakawa K. Expression of transient receptor potential channel vanilloid (TRPV) 1–4, melastin (TRPM) 5 and 8, and ankyrin (TRPA1) in the normal and methimazole-treated mouse olfactory epithelium. Acta Otolaryngol. 2010;130:1278–86.PubMedCentralPubMedCrossRef
33.
go back to reference Almirall J, Rofes L, Serra-Prat M, et al. Oropharyngeal dysphagia is a risk factor for community-acquired pneumonia in the elderly. Eur Respir J. 2013;41:923–8.PubMedCrossRef Almirall J, Rofes L, Serra-Prat M, et al. Oropharyngeal dysphagia is a risk factor for community-acquired pneumonia in the elderly. Eur Respir J. 2013;41:923–8.PubMedCrossRef
34.
go back to reference Cabre M, Serra-Prat M, Palomera E, Almirall J, Pallares R, Clave P. Prevalence and prognostic implications of dysphagia in elderly patients with pneumonia. Age Ageing. 2010;39:39–45.PubMedCrossRef Cabre M, Serra-Prat M, Palomera E, Almirall J, Pallares R, Clave P. Prevalence and prognostic implications of dysphagia in elderly patients with pneumonia. Age Ageing. 2010;39:39–45.PubMedCrossRef
35.
go back to reference Katzan IL, Cebul RD, Husak SH, Dawson NV, Baker DW. The effect of pneumonia on mortality among patients hospitalized for acute stroke. Neurology. 2003;60:620–5.PubMedCrossRef Katzan IL, Cebul RD, Husak SH, Dawson NV, Baker DW. The effect of pneumonia on mortality among patients hospitalized for acute stroke. Neurology. 2003;60:620–5.PubMedCrossRef
36.
go back to reference Hilker R, Poetter C, Findeisen N, et al. Nosocomial pneumonia after acute stroke: implications for neurological intensive care medicine. Stroke. 2003;34:975–81.PubMedCrossRef Hilker R, Poetter C, Findeisen N, et al. Nosocomial pneumonia after acute stroke: implications for neurological intensive care medicine. Stroke. 2003;34:975–81.PubMedCrossRef
37.
go back to reference Altman KW, Yu GP, Schaefer SD. Consequence of dysphagia in the hospitalized patient: impact on prognosis and hospital resources. Arch Otolaryngol Head Neck Surg. 2010;136:784–9.PubMedCrossRef Altman KW, Yu GP, Schaefer SD. Consequence of dysphagia in the hospitalized patient: impact on prognosis and hospital resources. Arch Otolaryngol Head Neck Surg. 2010;136:784–9.PubMedCrossRef
Metadata
Title
Effect of oral piperine on the swallow response of patients with oropharyngeal dysphagia
Authors
Laia Rofes
Viridiana Arreola
Alberto Martin
Pere Clavé
Publication date
01-12-2014
Publisher
Springer Japan
Published in
Journal of Gastroenterology / Issue 12/2014
Print ISSN: 0944-1174
Electronic ISSN: 1435-5922
DOI
https://doi.org/10.1007/s00535-013-0920-0

Other articles of this Issue 12/2014

Journal of Gastroenterology 12/2014 Go to the issue