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

 

 Buy Article Permissions and Reprints

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.

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
  PubMedGoogle Scholar
• 2 Kinney J M. Nutritional frailty, sarcopenia and falls in the elderly.  Curr Opin Clin Nutr Metab Care. 2004;  7 15-20
  PubMedGoogle Scholar
• 3 Robbins J, Hamilton J W, Lof G L, Kempster G. Oropharyngeal swallowing in normal adults of different ages.  Gastroenterology. 1992;  103 823-829
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 8 Evans W J. What is sarcopenia?.  J Gerontol A Biol Sci Med Sci. 1995;  50A 5-8
  PubMedGoogle Scholar
• 9 Fiatarone M A, Evans W J. The etiology and reversibility of muscle dysfunction in the aged.  J Gerontol. 1993;  48(Spec) 77-83
  PubMedGoogle Scholar
• 10 Price P A, Darvell B W. Force and mobility in the aging human tongue.  Med J Aust. 1981;  1 75-78
  PubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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;
  Google Scholar
• 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
  Google Scholar
• 17 Solomon N P. Changes in normal speech after fatiguing the tongue.  J Speech Lang Hear Res. 2000;  43 1416-1428
  PubMedGoogle Scholar
• 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
  Google Scholar
• 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
  PubMedGoogle Scholar
• 20 Macaluso A, DeVito G. Muscle strength, power and adaptations to resistance training in older people.  Eur J Appl Physiol. 2004;  91 450-472
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 22 Gandevia S C. Roles for perceived voluntary motor commands in motor control.  Trends Neurosci. 1987;  10 81-85
  CrossrefPubMedGoogle Scholar
• 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
  Google Scholar
• 24 Gandevia S C. Some central and peripheral factors affecting human motorneuronal output in neuromuscular fatigue.  Sports Med. 1992;  13 93-98
  PubMedGoogle Scholar
• 25 Levine R, Robbins J A, Maser A. Periventricular white matter changes and oropharyngeal swallowing in normal individuals.  Dysphagia. 1992;  7 142-147
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  Google Scholar
• 28 Sapienza C. Role of Strength Training. Presented at: the 13th Annual Meeting of Dysphagia Research Society 2004 Montreal, Canada;
  Google Scholar
• 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;
  Google Scholar
• 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
  Google Scholar
• 30 Rosenbek J C, Robbins J A, Roecker E B, Coyle J L, Wood J LA. Penetration-Aspiration Scale.  Dysphagia. 1996;  11 93-98
  Google Scholar
• 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
  Google Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 53 Sipila S, Suominen H. Muscle ultrasonography and computed tomography in elderly trained and untrained women.  Muscle Nerve. 1993;  16 294-300
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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;
  Google Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 62 Pouderoux P, Ergun G A, Lin S, Kahrilas P. Esophageal bolus transit image by ultrafast computerized tomography.  Gastroenterology. 1996;  110 1422-1428
  CrossrefPubMedGoogle Scholar
• 63 Sale D G. Neural adaptation to resistance training.  Med Sci Sports Exerc. 1988;  20 S135-S145
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 73 Martin R, Barr A, MacIntosh B et al.. Cerebral cortical processing of swallowing in older adults.  Exp Brain Res. 2006(Aug);  5
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar

Stephanie KaysM.S. 

William S. Middleton Memorial Veterans Hospital

2500 Overlook Terrace, GRECC, 11G, Madison, WI 53706

Email: sakays@wisc.edu