Age- and stroke-related skeletal muscle changes a review for the geriatric clinician

Journal of Geriatric Physical Therapy

Volumn 35, Issue 3, 2012, Pages 155-161

  Sions, Jaclyn Megan ^a   Tyrell, Christine M ^a   Knarr, Brian A ^a   Jancosko, Angela ^a   Binder Macleod, Stuart A ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

Aging; Intramuscular fat; Sarcopenia; Stroke

Indexed keywords

AGE; AGING; CEREBROVASCULAR ACCIDENT; DAILY LIFE ACTIVITY; GERIATRICS; HUMAN; METABOLISM; MUSCLE ATROPHY; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SKELETAL MUSCLE;

ACTIVITIES OF DAILY LIVING; AGE FACTORS; AGING; GERIATRICS; HUMANS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; STROKE;

EID: 84868277464     PISSN: 15398412     EISSN: 21520895     Source Type: Journal    
DOI: 10.1519/JPT.0b013e318236db92     Document Type: Article

References (103)

1. Kirshner HS, Biller J, Callahan AS III. Long-term therapy to prevent stroke. J Am Board Fam Pract. 2005;18(6):528-540.
2. Centers for Disease Control and P. Stroke facts and statistics. http://www.cdc.gov/stroke/stroke-facts.htm. Accessed November 19, 2008.
3. Buurke JH, Hermens HJ, Erren-Wolters CV, Nene AV. The effect of walking aids on muscle activation patterns during walking in stroke patients. Gait Posture. 2005;22(2):164-170.
4. Goldstein LB, Simel DL. Is this patient having a stroke? JAMA. 2005;293(19):2391-2402.
5. Zerwic JJ, Ennen K, De Von HA. Stroke. Risks, recognition, and return to work. AAOHN J. 2002;50(8):354-359.
6. Ustinova KI, Fung J, Levin MF. Disruption of bilateral temporal coordination during arm swinging in patients with hemiparesis. Exp Brain Res. 2006;169(2):194-207.
7. Lewis GN, Perreault EJ. Side of lesion influences bilateral activation in chronic, post-stroke hemiparesis. Clin Neurophysiol. 2007;118(9):2050-2062.
8. Vandervoort AA. Aging of the human neuromuscular system. Muscle Nerve. 2002;25(1):17-25.
9. Latash ML. Neurophysiological Basis of Movement. 2nd ed. Urbana, IL: Human Kinetics Publishers; 2008.
10. Kraemer WJ. Skeletal muscle physiology: plasticity and responses to exercise. Hormone Res. 2006;66(suppl 1):2-16.
11. Toffola ED, Sparpaglione D, Pistorio A, Buonocore M. Myoelectric manifestations of muscle changes in stroke patients. Arch Phys Med Rehabil. 2001;82(5):661-665.
12. McComas AJ, Sica RE, Upton AR, Aguilera N. Functional changes in motoneurones of hemiparetic patients. J Neurol Neurosurg Psychiatry. 1973;36(2):183-193.
13. Lee WS, Cheung WH, Qin L, Tang N, Leung KS. Age-associated decrease of type IIA/B human skeletal muscle fibers. Clin Orthop Relat Res. 2006;450:231-237.
14. Brunner F, Schmid A, Sheikhzadeh A, Nordin M, Yoon J, Frankel V. Effects of aging on Type II muscle fibers: a systematic review of the literature. J Aging Phys Act. 2007;15(3):336-348.
15. MacIntosh BR, Gardiner PF, McComas AJ. Skeletal Muscle: Form and Function. 2nd ed. Champaign, IL: Human Kinetics Publishers; 2006.
16. Kernell D. Principles of force gradation in skeletal muscles. Neural Plast. 2003;10 (1-2):69-76.
17. Celichowski J. Mechanisms underlying the regulation of motor unit contraction in the skeletal muscle. J Physiol Pharmacol. 2000;51(1):17-33.
18. Faulkner JA, Larkin LM, Claflin DR, Brooks SV. Age-related changes in the structure and function of skeletal muscles. Clin Exp Pharmacol Physiol. 2007;34(11):1091-1096.
19. Lexell J, Taylor CC, Sjostrom M. What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15-to 83-year-old men. J Neurol Sci. 1988;84 (2-3):275-294.
20. Maughan RJ, Watson JS, Weir J. Strength and cross-sectional area of human skeletal muscle. J Physiol. 1983;338:37-49.
21. Jubrias SA, Odderson IR, Esselman PC, Conley KE. Decline in isokinetic force with age: muscle cross-sectional area and specific force. Pflugers Arch. 1997;434(3):246-253.
22. Doherty TJ. Invited review: aging and sarcopenia. J Appl Physiol. 2003;95(4):1717-1727.
23. Frontera WR, Hughes VA, Fielding RA, Fiatarone MA, Evans WJ, Roubenoff R. Aging of skeletal muscle: a 12-yr longitudinal study. J Appl Physiol. 2000;88(4):1321-1326.
24. Visser M, Kritchevsky SB, Goodpaster BH, et al. Leg muscle mass and composition in relation to lower extremity performance in men and women aged 70 to 79: the health, aging and body composition study. J Am Geriatr Soc. 2002;50(5):897-904.
25. Hvid LG, Aagaard P, Justesen L, et al. Effects of aging on muscle mechanical function and muscle fiber morphology during short-term immobilization and subsequent retraining. J Appl Physiol. 2010;109(6):1628-1634.
26. Park H, Park S, Shephard RJ, Aoyagi Y. Yearlong physical activity and sarcopenia in older adults: the Nakanojo Study. Eur J Appl Physiol. 2010;109(5):953-961.
27. Chien M Y, Kuo HK, Wu Y T. Sarcopenia, cardiopulmonary fitness, and physical disability in community-dwelling elderly people. Phys Ther. 2010;90(9):1277-1287.
28. Physical activity and cardiovascular health. NIH consensus development panel on physical activity and cardiovascular health. JAMA. 1996;276(3):241-246.
29. Suetta C, Andersen JL, Dalgas U, et al. Resistance training induces qualitative changes in muscle morphology, muscle architecture, and muscle function in elderly postoperative patients. J Appl Physiol. 2008;105(1):180-186.
30. Holviala JH, Sallinen JM, Kraemer WJ, Alen MJ, Hakkinen KK. Effects of strength training on muscle strength characteristics, functional capabilities, and balance in middle-aged and older women. J Strength Cond Res. 2006;20(2):336-344.
31. Hachisuka K, Umezu Y, Ogata H. Disuse muscle atrophy of lower limbs in hemiplegic patients. Arch Phys Med Rehabil. 1997;78(1):13-18.
32. Scelsi R, Lotta S, Lommi G, Poggi P, Marchetti C. Hemiplegic atrophy. Morphological findings in the anterior tibial muscle of patients with cerebral vascular accidents. Acta Neuropathol. 1984;62(4):324-331.
33. Bohannon RW. Knee extension strength and body weight determine sit-to-stand independence after stroke. Physiother Theory Pract. 2007;23(5):291-297.
34. Cheng PT, Chen CL, Wang CM, Hong WH. Leg muscle activation patterns of sit-to-stand movement in stroke patients. Am J Phys Med Rehabil. 2004;83(1):10-16.
35. Kim CM, Eng JJ. The relationship of lower-extremity muscle torque to locomotor performance in people with stroke. Phys Ther. 2003;83(1):49-57.
36. Marigold DS, Eng JJ, Tokuno CD, Donnelly CA. Contribution of muscle strength and integration of afferent input to postural instability in persons with stroke. Neurorehabil Neural Repair. 2004;18(4):222-229.
37. Ryan AS, Dobrovolny CL, Smith GV, Silver KH, Macko R F. Hemiparetic muscle atrophy and increased intramuscular fat in stroke patients. Arch Phys Med Rehabil. 2002;83(12):1703-1707.
38. Metoki N, Sato Y, Satoh K, Okumura K, Iwamoto J. Muscular atrophy in the hemiplegic thigh in patients after stroke. Am J Phys Med Rehabil. 2003;82(11):862-865.
39. Ploutz-Snyder LL, Clark BC, Logan L, Turk M. Evaluation of spastic muscle in stroke survivors using magnetic resonance imaging and resistance to passive motion. Arch Phys Med Rehabil. 2006;87(12):1636-1642.
40. Sunderland A, Bowers MP, Sluman SM, Wilcock DJ, Ardron ME. Impaired dexterity of the ipsilateral hand after stroke and the relationship to cognitive deficit. Stroke. 1999;30(5):949-955.
41. Desrosiers J, Bourbonnais D, Bravo G, Roy PM, Guay M. Performance of the 'unaffected' upper extremity of elderly stroke patients. Stroke. 1996;27(9):1564-1570.
42. Noskin O, Krakauer JW, Lazar RM, et al. Ipsilateral motor dysfunction from unilateral stroke: implications for the functional neuroanatomy of hemiparesis. J Neurol Neurosurg Psychiatry. 2008;79(4):401-406.
43. Baskett JJ, Marshall HJ, Broad JB, Owen PH, Green G. The good side after stroke: ipsilateral sensory-motor function needs careful assessment. Age Ageing. 1996;25(3):239-244.
44. Andrews AW, Bohannon RW. Distribution of muscle strength impairments following stroke. Clin Rehabil. 2000;14(1):79-87.
45. Jorgensen L, Jacobsen BK. Changes in muscle mass, fat mass, and bone mineral content in the legs after stroke: a 1 year prospective study. Bone. 2001;28(6):655-659.
46. Delmonico MJ, Harris TB, Visser M, et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. 2009;90(6):1579-1585.
47. Delbono O. Neural control of aging skeletal muscle. Aging Cell. 2003;2(1):21-29.
48. Kanda K, Hashizume K. Effects of long-term physical exercise on age-related changes of spinal motoneurons and peripheral nerves in rats. Neurosci Res. 1998;31(1):69-75.
49. Kawabuchi M, Zhou CJ, Wang S, Nakamura K, Liu WT, Hirata K. The spatiotemporal relationship among Schwann cells, axons and postsynaptic acetylcholine receptor regions during muscle reinnervation in aged rats. Anat Rec. 2001;264(2):183-202.
50. Kirkendall DT, Garrett WE Jr. The effects of aging and training on skeletal muscle. Am J Sports Med. 1998;26(4):598-602.
51. Song MY, Ruts E, Kim J, Janumala I, Heymsfield S, Gallagher D. Sarcopenia and increased adipose tissue infiltration of muscle in elderly African American women. Am J Clin Nutr. 2004;79(5):874-880.
52. Hara Y, Masakado Y, Chino N. The physiological functional loss of single thenar motor units in the stroke patients: when does it occur? Does it progress? Clin Neurophysiol. 2004;115(1):97-103.
53. Lukacs M, Vecsei L, Beniczky S. Changes in muscle fiber density following a stroke. Clin Neurophysiol. 2009;120(8):1539-1542.
54. Gallagher D, Kuznia P, Heshka S, et al. Adipose tissue in muscle: a novel depot similar in size to visceral adipose tissue. Am J Clin Nutr. 2005;81(4):903-910.
55. Danneels LA, Vanderstraeten GG, Cambier DC, Witvrouw EE, De Cuyper HJ. CT imaging of trunk muscles in chronic low back pain patients and healthy control subjects. Eur Spine J. 2000;9(4):266-272.
56. Miljkovic-Gacic I, Wang X, Kammerer CM, et al. Fat infiltration in muscle: new evidence for familial clustering and associations with diabetes. Obesity (Silver Spring). 2008;16(8):1854-1860.
57. Ryan AS, Nicklas BJ. Age-related changes in fat deposition in mid-thigh muscle in women: relationships with metabolic cardiovascular disease risk factors. Int J Obes Relat Metab Disord. 1999;23(2):126-132.
58. Hadar H, Gadoth N, Heifetz M. Fatty replacement of lower paraspinal muscles: normal and neuromuscular disorders. AJR Am J Roentgenol. 1983;141(5):895-898.
59. Ryall JG, Schertzer JD, Lynch GS. Cellular and molecular mechanisms underlying age-related skeletal muscle wasting and weakness. Biogerontology. 2008;9(4):213-228.
60. Van Loon LJ. Use of intramuscular triacylglycerol as a substrate source during exercise in humans. J Appl Physiol. 2004;97(4):1170-1187.
61. Schrauwen-Hinderling VB, Kooi ME, Hesselink MK, et al. Intramyocellular lipid content and molecular adaptations in response to a 1-week high-fat diet. Obes Res. 2005;13(12):2088-2094.
62. Hwang JH, Pan JW, Heydari S, Hetherington H P, Stein DT. Regional differences in intramyocellular lipids in humans observed by in vivo 1H-MR spectroscopic imaging. J Appl Physiol. 2001;90(4):1267-1274.
63. Taaffe DR, Henwood TR, Nalls MA, Walker DG, Lang T F, Harris TB. Alterations in muscle attenuation following detraining and retraining in resistancetrained older adults. Gerontology. 2009;55(2):217-223.
64. Hicks GE, Simonsick EM, Harris TB, et al. Trunk muscle composition as a predictor of reduced functional capacity in the health, aging and body composition study: the moderating role of back pain. J Gerontol A Biol Sci Med Sci. 2005;60(11):1420-1424.
65. Visser M, Goodpaster BH, Kritchevsky SB, et al. Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in wellfunctioning older persons. J Gerontol A Biol Sci Med Sci. 2005;60(3):324-333.
66. Kent-Braun JA, Ng AV, Young K. Skeletal muscle contractile and noncontractile components in young and older women and men. J Appl Physiol. 2000;88(2):662-668.
67. Johannsen DL, Ravussin E. Obesity in the elderly: is faulty metabolism to blame? Aging health. 2010;6(2):159-167.
68. Halloszy J, McArdle WD, Katch FI, Katch VL. Energy Transfer in the Body. Vol 5. Baltimore, MD: Lippincott Williams & Wilkins; 2001:131-173.
69. Ravussin E, Smith SR. Increased fat intake, impaired fat oxidation, and failure of fat cell proliferation result in ectopic fat storage, insulin resistance, and type 2 diabetes mellitus. Ann N Y Acad Sci. 2002;967:363-378.
70. White LJ, Ferguson MA, McCoy SC, Kim H. Intramyocellular lipid changes in men and women during aerobic exercise: a (1) H-magnetic resonance spectroscopy study. J Clin Endocrinol Metab. 2003;88(12):5638-5643.
71. Short KR, Vittone JL, Bigelow ML, Proctor DN, Nair KS. Age and aerobic exercise training effects on whole body and muscle protein metabolism. Am J Physiol Endocrinol Metab. 2004;286(1):E92-E101.
72. Guadagni M, Biolo G. Effects of inflammation and/or inactivity on the need for dietary protein. Curr Opin Clin Nutr Metab Care. 2009;12(6):617-622.
73. Chernoff R. Protein and older adults. J Am Coll Nutr. 2004;23(suppl 6):627S-630S.
74. Baumgartner RN, Wayne SJ, Waters DL, Janssen I, Gallagher D, Morley JE. Sarcopenic obesity predicts instrumental activities of daily living disability in the elderly. Obes Res. 2004;12(12):1995-2004.
75. Goodpaster BH, Carlson CL, Visser M, et al. Attenuation of skeletal muscle and strength in the elderly: The Health ABC Study. J Appl Physiol. 2001;90(6):2157-2165.
76. De Castro Rodrigues A, Andreo JC, Rosa GM Jr, Dos Santos NB, Moraes LH, Lauris JR. Fat cell invasion in long-term denervated skeletal muscle. Microsurgery. 2007;27(8):664-667.
77. Suetta C, Magnusson S P, Rosted A, et al. Resistance training in the early postoperative phase reduces hospitalization and leads to muscle hypertrophy in elderly hip surgery patients-a controlled, randomized study. J Am Geriatr Soc. 2004;52(12):2016-2022.
78. Martel G F, Roth SM, Ivey FM, et al. Age and sex affect human muscle fibre adaptations to heavy-resistance strength training. Exp Physiol. 2006;91(2):457-464.
79. Nakai R, Azuma T, Sudo M, Urayama S, Takizawa O, Tsutsumi S. MRI analysis of structural changes in skeletal muscles and surrounding tissues following long-term walking exercise with training equipment. J Appl Physiol. 2008;105(3):958-963.
80. Kukuljan S, Nowson CA, Sanders K, Daly RM. Effects of resistance exercise and fortified milk on skeletal muscle mass, muscle size, and functional performance in middle-aged and older men: an 18-mo randomized controlled trial. J Appl Physiol. 2009;107(6):1864-1873.
81. Hanson ED, Srivatsan SR, Agrawal S, et al. Effects of strength training on physical function: influence of power, strength, and body composition. J Strength Cond Res. 2009;23(9):2627-2637.
82. Koppenhaver SL, Hebert JJ, Fritz JM, Parent EC, Teyhen DS, Magel JS. Reliability of rehabilitative ultrasound imaging of the transversus abdominis and lumbar multifidus muscles. Arch Phys Med Rehabil. 2009;90(1):87-94.
83. Koppenhaver SL, Hebert JJ, Parent EC, Fritz JM. Rehabilitative ultrasound imaging is a valid measure of trunk muscle size and activation during most isometric sub-maximal contractions: a systematic review. Aust J Physiother. 2009;55(3):153-169.
84. Teyhen D. Rehabilitative Ultrasound Imaging Symposium San Antonio, TX, May 8-10, 2006. J Orthop Sports Phys Ther. 2006;36(8):A1-A3.
85. Ryan AS, Ivey FM, Prior S, Li G, Hafer-Macko C. Skeletal muscle hypertrophy and muscle myostatin reduction after resistive training in stroke survivors. Stroke. 2011;42(2):416-420.
86. Bohannon RW. Muscle strength and muscle training after stroke. J Rehabil Med. 2007;39(1):14-20.
87. Weiss A, Suzuki T, Bean J, Fielding RA. High intensity strength training improves strength and functional performance after stroke. Am J Phys Med Rehabil. 2000;79(4):369-376.
88. Ouellette MM, Le Brasseur NK, Bean JF, et al. High-intensity resistance training improves muscle strength, self-reported function, and disability in longterm stroke survivors. Stroke. 2004;35(6):1404-1409.
89. Sharp SA, Brouwer BJ. Isokinetic strength training of the hemiparetic knee: effects on function and spasticity. Arch Phys Med Rehabil. 1997;78(11):1231-1236.
90. Van Peppen RP, Kwakkel G, Wood-Dauphinee S, Hendriks HJ, Van Der Wees PJ, Dekker J. The impact of physical therapy on functional outcomes after stroke: what's the evidence? Clin Rehabil. 2004;18(8):833-862.
91. Rose D, Paris T, Crews E, et al. Feasibility and effectiveness of circuit training in acute stroke rehabilitation. Neurorehabil Neural Repair. 2011;25(2):140-148.
92. Management of Stroke Rehabilitation Working Group. VA/DOD Clinical practice guideline for the management of stroke rehabilitation. J Rehabil Res Dev. 2010;47(9):1-43.
93. Delitto A, Snyder-Mackler L. Two theories of muscle strength augmentation using percutaneous electrical stimulation. Phys Ther. 1990;70(3):158-164.
94. Petterson S, Snyder-Mackler L. The use of neuromuscular electrical stimulation to improve activation deficits in a patient with chronic quadriceps strength impairments following total knee arthroplasty. J Orthop Sports Phys Ther. 2006;36(9):678-685.
95. Marqueste T, Hug F, Decherchi P, Jammes Y. Changes in neuromuscular function after training by functional electrical stimulation. Muscle Nerve. 2003;28(2):181-188.
96. Macko RF, Ivey FM, Forrester LW, et al. Treadmill exercise rehabilitation improves ambulatory function and cardiovascular fitness in patients with chronic stroke: a randomized, controlled trial. Stroke. 2005;36(10):2206-2211.
97. Moseley AM, Stark A, Cameron ID, Pollock A. Treadmill training and body weight support for walking after stroke. Cochrane Database Syst Rev. 2005; (4): CD002840.
98. Visintin M, Barbeau H, Korner-Bitensky N, Mayo NE. A new approach to retrain gait in stroke patients through body weight support and treadmill stimulation. Stroke. 1998;29(6):1122-1128.
99. Barbeau H, Visintin M. Optimal outcomes obtained with body-weight support combined with treadmill training in stroke subjects. Arch Phys Med Rehabil. 2003;84(10):1458-1465.
100. Ivey FM, Hafer-Macko CE, Macko RF. Task-oriented treadmill exercise training in chronic hemiparetic stroke. J Rehabil Res Dev. 2008;45(2):249-259.
101. Hesse S. Treadmill training with partial body weight support after stroke: a review. Neuro Rehabilitation. 2008;23(1):55-65.
102. McCain KJ, Pollo FE, Baum BS, Coleman SC, Baker S, Smith PS. Locomotor treadmill training with partial body-weight support before overground gait in adults with acute stroke: a pilot study. Arch Phys Med Rehabil. 2008;89(4):684-691.
103. McCain KJ, Smith PS. Locomotor treadmill training with body-weight support prior to over-ground gait: promoting symmetrical gait in a subject with acute stroke. Top Stroke Rehabil. 2007;14(5):18-27.