Effects of Sensorimotor Exercise on Swallowing Outcomes Relative to Age and Age-Related Disease

Abstract

Parallel to the growing number of adults over age 65 years and the increasing use of exercise in geriatric medicine to improve function and decrease fall risk, recent advances in the treatment of geriatric dysphagia have focused on rehabilitating swallowing function with active exercise. Specific changes in central neural pathways as well as peripheral end organs (muscles) that occur with natural aging may predispose older adults to an increased risk for dysphagia when faced with chronic medical conditions. Research to date primarily has focused on the utility of nonswallow motor exercises to increase muscle strength and range of motion in oropharyngeal structures. Future directions in the field of dysphagia rehabilitation demand evidence-based investigations into the ability of exercise to affect neural plasticity, representing long-lasting alterations in neural organization.

KEYWORDS

Exercise - strengthening - dysphagia intervention - aged swallowing

REFERENCES

• 1 Winograd C H, Gerety M D, Chung M, Goldstein M K, Dominques F, Vallone R. Screening for frailty: criteria and predictors of outcomes.  J Am Geriatr Soc. 1991;  39 778-784
• 2 Kinney J M. Nutritional frailty, sarcopenia and falls in the elderly.  Curr Opin Clin Nutr Metab Care. 2004;  7 15-20
• 3 Robbins J, Hamilton J W, Lof G L, Kempster G. Oropharyngeal swallowing in normal adults of different ages.  Gastroenterology. 1992;  103 823-829
• 4 Tracy J F, Logemann J A, Kahrilas P J, Jacob P, Kobara M, Krug C. Preliminary observations on the effects of age on oropharyngeal deglutition.  Dysphagia. 1989;  4 90-94
• 5 Shaw D W, Cook I J, Dent J et al.. Age influences oropharyngeal and upper esophageal sphincter function during swallowing.  Gastroenterology. 1990;  98 A390
• 6 Shaw D W, Cook I J, Gabb M et al.. Influence of normal aging on oropharyngeal and upper esophageal sphincter function during swallow.  Am J Physiol. 1995;  L68 G389-G390
• 7 Fiatarone M A, Marks E C, Ryan N D, Meredith C N, Lipsitz L A, Evans W J. High intensity strength training in non-agenarians. Effects on skeletal muscle.  JAMA. 1990;  263 3029-3034
• 8 Evans W J. What is sarcopenia?.  J Gerontol A Biol Sci Med Sci. 1995;  50A 5-8
• 9 Fiatarone M A, Evans W J. The etiology and reversibility of muscle dysfunction in the aged.  J Gerontol. 1993;  48(Spec) 77-83
• 10 Price P A, Darvell B W. Force and mobility in the aging human tongue.  Med J Aust. 1981;  1 75-78
• 11 Newton J P, Abel R W, Robertson E M, Yemm R. Changes in human masseter and medial pterygoid muscles with age: a study by computed tomography.  Gerodontics. 1987;  3 151-154
• 12 Robbins J, Gangnon R, Theis S, Kays S A, Hind J. The effects of lingual exercise on swallowing in older adults.  J Am Geriatr Soc. 2005;  53 1483-1489
• 13 Robbins J, Levine R, Wood J, Roecker E, Luschei E. Age effects on lingual pressure generation as a risk factor for dysphagia.  J Gerontol A Biol Sci Med Sci. 1995;  50 M257-M262
• 14 Nicosia M A, Hind J A, Roecker E B, Carnes M, Robbins J A. Age effects on the temporal evolution of isometric and swallowing pressure.  J Gerontol A Biol Sci Med Sci. 2000;  55A M634-M640
• 15 Nagai H, Russell J A, Jackson M, Konopacki R, Connor N P. Alterations in protrusive tongue muscle forces in aged rats. American Academy of Otolaryngology-Head and Neck Surgery Foundation September 19-22, 2004 New York, NY;
• 16 Narici M. Effect of ageing on muscle contractile properties. In: Capodaglio P, Narici MV Advances in Rehabilitation. Physical Activity in the Elderly. Pavia; Maugeri Foundation Books and PI-ME Press 1999: 61-67
• 17 Solomon N P. Changes in normal speech after fatiguing the tongue.  J Speech Lang Hear Res. 2000;  43 1416-1428
• 18 Narici M V, Roi G S, Landoni L, Minetti A E, Ceretelli P. Changes in force, cross-sectional area, and neural activation during strength training and detraining of the human quadriceps.  Eur J Appl Physiol Occup Physiol. 1989;  59 310-319
• 19 Phillips S K, Bruce S A, Newton D, Woledge R C. The weakness of old age is not due to failure of muscle activation.  J Gerontol. 1992;  47 M45-M49
• 20 Macaluso A, DeVito G. Muscle strength, power and adaptations to resistance training in older people.  Eur J Appl Physiol. 2004;  91 450-472
• 21 Solomon N P, Robin D A, Mitchinson S I, Vandaele D J, Luschei E S. Sense of effort and the effects of fatigue in the tongue and hand.  J Speech Hear Res. 1996;  39 114-125
• 22 Gandevia S C. Roles for perceived voluntary motor commands in motor control.  Trends Neurosci. 1987;  10 81-85
• 23 McCloskey D I, Gandevia S C, Potter E K, Colebatch J G. Muscle sense and effort: Motor commands and judgements about muscular contractions. In: Desmedt JE Motor Control Mechanisms in Health and Disease. New York; Raven Press 1983: 151-167
• 24 Gandevia S C. Some central and peripheral factors affecting human motorneuronal output in neuromuscular fatigue.  Sports Med. 1992;  13 93-98
• 25 Levine R, Robbins J A, Maser A. Periventricular white matter changes and oropharyngeal swallowing in normal individuals.  Dysphagia. 1992;  7 142-147
• 26 Lazarus C, Logemann J, Huang C, Rademaker A. Effects of two types of tongue strengthening exercises in young normals.  Folia Phoniatr Logop. 2003;  55 199-205
• 27 Shaker R, Easterling C, Kern M et al.. Rehabilitation of swallowing by exercise in tube-fed patients with pharyngeal dysphagia secondary to abnormal UES opening.  Gastroenterology. 2002;  122 1314-1321
• 28 Sapienza C. Role of Strength Training. Presented at: the 13th Annual Meeting of Dysphagia Research Society 2004 Montreal, Canada;
• 29 Kim J, Sapienza C, Davenport P. Expiratory muscle strength training for the elderly: a preliminary study. Presented at: the annual meeting of the American Speech Hearing and Language Association 2005 San Diego, CA;
• 29a Robbins J A, Kay S A, Gangnon R E et al.. The effects of lingual exercise in stroke patients with dysphagia. Arch Phys Med Rehabil 2006 In press
• 30 Rosenbek J C, Robbins J A, Roecker E B, Coyle J L, Wood J LA. Penetration-Aspiration Scale.  Dysphagia. 1996;  11 93-98
• 31 Robbins J, Coyle J, Roecker E, Rosenbek J, Wood J. Differentiation of normal and abnormal airway protection during swallowing using the penetration-aspiration scale.  Dysphagia. 1999;  14 228-232
• 32 Shaker R, Kern M, Bardan E et al.. Augmentation of deglutitive upper esophageal sphincter opening in the elderly by exercise.  Am J Physiol. 1997;  272 G1518-G1522
• 33 Hamdy S, Rothwell J C, Aziz Q, Singh K, Thompson D G. Long-term reorganization of human motor cortex driven by short-term sensory stimulation.  Nat Neurosci. 1998;  1 64-68
• 34 Power M, Fraser C, Hobson A et al.. Changes in pharyngeal corticobulbar excitability and swallowing behavior after oral stimulation.  Am J Physiol Gastrointest Liver Physiol. 2004;  286 G45-G50
• 35 McDonagh M J, Davies C T. Adaptive response of mammalian skeletal muscle to exercise with high loads.  Eur J Appl Physiol Occup Physiol. 1984;  52 139-155
• 36 Racine R J, Chapman C A, Trepel C, Teskey G C, Milgram N W. Post-activation potentiation in the neocortex. IV. Multiple sessions required for induction of the long-term potentiation in the chronic preparation in the chronic preparation.  Brain Res. 1995;  702 87-93
• 37 Frontera W R, Meredith C N, O'Reilly K P, Knuttgen H G, Evan W J. Strength conditioning in older men: skeletal muscle hypertrophy and improved function.  J Appl Physiol. 1988;  64 1038-1044
• 38 Kraemer W J, Adams K, Carafelli E et al.. Progression models in resistance training for healthy adults. American College of Sports Medicine position stand.  Med Sci Sports Exerc. 2002;  34 364-380
• 39 Easterling C, Grande B, Kern M, Sears K, Shaker R. Attaining and maintaining isometric and isokenetic goals of the Shaker exercise.  Dysphagia. 2005;  20 133-138
• 40 Saleem A F, Sapienza C M, Okun M S. Respiratory muscle strength training: treatment and response duration in a patient with early idiopathic Parkinson's disease.  NeuroRehabilitation. 2005;  20 323-333
• 41 Cuoco A, Callahan D M, Sayers S et al.. Impact on muscle power and force on gait speed in disabled older men and women.  J Gerontol A Biol Sci Med Sci. 2004;  59A 1200-1206
• 42 Sayers S P, Guralnik J M, Thombs L A et al.. Effect of leg muscle contraction velocity on functional performance in older men and women.  J Am Geriatr Soc. 2005;  53 467-471
• 43 Hruda K, Hicks A L, McCartney N. Training for muscle power in older adults: effects on functional abilities.  Can J Appl Physiol. 2003;  28 178-189
• 44 Earles D R, Judge J O, Gunnarson O T. Velocity training induces power-specific adaptations in highly functioning older adults.  Arch Phys Med Rehabil. 2001;  82 872-878
• 45 Biernaskie J, Chernenko G, Corbett D. Efficacy of rehabilitative experience declines with time after focal ischemic brain injury.  J Neurosci. 2004;  24 1245-1254
• 46 Hakkinen K, Newton R U, Gordon S E et al.. Changes in muscle morphology, electromyographic activity, and force production characteristics during progressive strength training in young and older men.  J Gerontol A Biol Sci Med Sci. 1998;  53A B415-B423
• 47 Toraman N F. Short term and long term detraining: is there any difference between young-old and old people?.  Br J Sports Med. 2005;  39 561-564
• 48 Lemmer J T, Hurlbut D E, Martel G F. Age and gender responses to strength training and detraining.  Med Sci Sports Exerc. 2000;  32 1505-1512
• 49 Fatouros I G, Kambas A, Katrabas I et al.. Strength training and detraining effects on muscular strength, anaerobic power, and mobility of inactive older men are intensity dependent.  Br J Sports Med. 2005;  39 776-780
• 50 Trappe S, Williamson D, Godard M. Maintenance of whole muscle strength and size following resistance training older men.  J Gerontol A Biol Sci Med Sci. 2002;  57 B138-B143
• 51 Shawker T, Sonies B C, Hall T E et al.. Ultrasound analysis of the tongue, hyoid and larynx activity during swallowing.  Invest Radiol. 1984;  19 82-86
• 52 Reimers C D, Fleckenstein J L, Witt T N et al.. Muscular ultrasound in idiopathic inflammatory myopathies of adults.  J Neurol Sci. 1993;  116 82-92
• 53 Sipila S, Suominen H. Muscle ultrasonography and computed tomography in elderly trained and untrained women.  Muscle Nerve. 1993;  16 294-300
• 54 Sipila S, Suominen H. Quantitative ultrasonography of muscle: detection of adaptations to training in elderly women.  Arch Phys Med Rehabil. 1996;  77 1173-1178
• 55 Chi-Fisherman G, Hicks J E, Cintas H M, Sonies B C, Gerber L H. Ultrasound imaging distinguishes between normal and weak muscle.  Arch Phys Med Rehabil. 2004;  85 980-986
• 56 Miller J L. Ultrasound and the aerodigestive system: the research past, the imaging present, and the clinical future. Presented at: 14th Annual Meeting of the Dysphagia Research Society 2006 Scottsdale, AZ;
• 57 Gilbert R J, Napadow V J. Three-dimensional muscular architecture of the human tongue determined in vivo with diffusion tensor magnetic resonance imaging.  Dysphagia. 2005;  20 1-7
• 58 Ajaj W, Goyen M, Herrmann B et al.. Measuring tongue volume and visualizing the chewing and swallowing process using real-time TrueFISP imaging-initial clinical experience in healthy volunteers and patients with acromegaly.  Eur Radiol. 2005;  15 913-918
• 59 Kim S M, McCulloch T M, Rim K. Pharyngeal pressure analysis by the finite element method during liquid bolus swallow.  Ann Otol Rhinol Laryngol. 2000;  109 585-589
• 60 Lin S, Chen J, Hertz P, Kahrilas P. Dynamic reconstruction of the oropharyngeal swallow using computer based animation.  Comput Med Imaging Graph. 1996;  20 69-75
• 61 Ergun G A, Kahrilas P J, Lin S, Logemann J A, Harig J M. Shape, volume, and content of the deglutitive pharyngeal chamber imaged by ultrafast computerized tomography.  Gastroenterology. 1993;  105 1396-1403
• 62 Pouderoux P, Ergun G A, Lin S, Kahrilas P. Esophageal bolus transit image by ultrafast computerized tomography.  Gastroenterology. 1996;  110 1422-1428
• 63 Sale D G. Neural adaptation to resistance training.  Med Sci Sports Exerc. 1988;  20 S135-S145
• 64 Erim Z, Beg M F, Burke D T, deLuca C J. Effects of aging on motor-unit control properties.  J Neurophysiol. 1999;  82 2081-2091
• 65 Palmer P M, McCulloch T M, Jaffe D, Neel A T. Effects of a sour bolus on the intramuscular electromyographic (EMG) activity of muscles in the submental region.  Dysphagia. 2005;  20 210-217
• 66 Ding R, Logemann J A, Larson C R, Rademaker A W. The effects of taste and consistency on swallow physiology in younger and older healthy individuals: a surface electromyographic study.  J Speech Lang Hear Res. 2003;  46 977-989
• 67 Hamdy S, Mikulis D J, Crawley A, Xue S, Henry S, Diamant N E. Cortical activation during human volitional swallowing: an event-related fMRI study.  Am J Physiol. 1999;  277 G219-G225
• 68 Martin R E, Goodyear B G, Gati J S, Menon R S. Cerebral cortical representation of automatic and volitional swallowing in humans.  J Neurophysiol. 2001;  85 938-950
• 69 Suzuki M, Asada Y, Ito J, Hayashi K, Inoue H, Kitano H. Activation of the cerebellum and basal ganglia on volitional swallowing detected by functional magnetic resonance imaging.  Dysphagia. 2003;  18 71-77
• 70 Kern M K, Jaradeh S, Arndorfer R C, Shaker R. Cerebral cortical representation of reflexive and volitional swallowing in humans.  Am J Physiol Gastrointest Liver Physiol. 2001;  280 G354-G360
• 71 Watanabe Y, Abe S, Ishikawa T, Yamada Y, Yamane G Y. Cortical regulation during the early stage of initiation of voluntary swallowing in humans.  Dysphagia. 2004;  19 100-108
• 72 Martin R E, MacIntosh B J, Smith R C et al.. Cerebral areas processing swallowing and tongue movement are overlapping but distinct: a functional magnetic resonance imaging study.  J Neurophysiol. 2004;  92 2428-2443
• 73 Martin R, Barr A, MacIntosh B et al.. Cerebral cortical processing of swallowing in older adults.  Exp Brain Res. 2006(Aug);  5
• 74 Ward N S, Brown M M, Thompson A J, Frackowiak R S. Neural correlates of motor recovery after stroke: a longitudinal fMRI study.  Brain. 2003;  126 2476-2496
• 75 Hamdy S, Xue S, Valdez D, Diamant N E. Induction of cortical swallowing activity by transcranial magnetic stimulation in the anaesthetized cat.  Neurogastroenterol Motil. 2001;  13 65-72
• 76 Gow D, Hobson A R, Furlong P, Hamdy S. Characterising the central mechanisms of sensory modulation in human swallowing motor cortex.  Clin Neurophysiol. 2004;  115 2382-2390
• 77 Hamdy S, Aziz Q, Rothwell J C, Hobson A, Thompson D G. Sensorimotor modulation of human cortical swallowing pathways.  J Physiol. 1998;  506 857-866
• 78 Gow D, Rothwell J, Hobson A, Thompson D, Hamdy S. Induction of long-term plasticity in human swallowing motor cortex following repetitive cortical stimulation.  Clin Neurophysiol. 2004;  115 1044-1051
• 79 Fraser C, Power M, Hamdy S et al.. Driving plasticity in adult human motor cortex is associated with improved motor function after brain injury.  Neuron. 2002;  34 831-840