Sports Medicine

, Volume 41, Issue 4, pp 289–306 | Cite as

Strength Training as a Countermeasure to Aging Muscle and Chronic Disease

  • Ben F. Hurley
  • Erik D. Hanson
  • Andrew K. Sheaff
Review Article

Abstract

Strength training (ST) has long been considered a promising intervention for reversing the loss of muscle function and the deterioration of muscle structure associated with advanced age but, until recently, the evidence was insufficient to support its role in the prevention or treatment of disease. In recent decades, there has been a long list of quality reviews examining the effects of ST on functional abilities and a few on risk factors for specific diseases, but none have provided a comprehensive assessment of ST as an intervention for a broad range of diseases. This review provides an overview of research addressing the effectiveness of ST as an intervention for the prevention or treatment of the adverse consequences of (i) aging muscle; (ii) the metabolic syndrome (MetS) and its components, i.e. insulin resistance, abdominal obesity, hyperlipidaemia and hypertension; (iii) fibromyalgia; (iv) rheumatoid arthritis; and (v) Alzheimer’s disease. Collectively, these studies indicate that ST may serve as an effective countermeasure to some of the adverse consequences of the MetS, fibromyalgia and rheumatoid arthritis.

Evidence in support of the hypothesis that ST reduces insulin resistance or improves insulin action comes both from indirect biomarkers, such as glycosylated haemoglobin (HbA1c), and insulin responses to oral glucose tolerance tests, as well as from more direct procedures such as hyperglycaemic and hyperinsulinaemic-euglycaemic clamp techniques. The evidence for the use of ST as a countermeasure of abdominal obesity is less convincing. Although some reports show statistically significant reductions in visceral fat, it is unclear if the magnitude of these changes are physiologically meaningful and if they are independent of dietary influences. The efficacy of ST as an intervention for reducing dyslipidaemia is at best inconsistent, particularly when compared with other pharmacological and non-pharmacological interventions, such as aerobic exercise training. However, there is more consistent evidence for the effectiveness of ST in reducing triglyceride levels. This finding could have clinical significance, given that elevated triglyceride is one of the five criterion measures for the diagnosis of the MetS. Small to moderate reductions in resting and exercise blood pressure have been reported with some indication that this effect may be genotype dependent. ST improves or reverses some of the adverse effects of fibromyalgia and rheumatoid arthritis, particularly pain, inflammation, muscle weakness and fatigue. Investigations are needed to determine how these effects compare with those elicited from aerobic exercise training and/or standard treatments. There is no evidence that ST can reverse any of the major biological or behavioural outcomes of Alzheimer’s disease, but there is evidence that the prevalence of this disease is inversely associated with muscle mass and strength. Some indicators of cognitive function may also improve with ST.

Thus, ST is an effective countermeasure for some of the adverse effects experienced by patients of many chronic diseases, as discussed in this review.

References

  1. 1.
    Danaei G, Ding Eric L, Mozaffarian D, et al. The preventable causes of death in the United States: comparativerisk assessment of dietary, lifestyle, and metabolic riskfactors. PloS Med 2009; 6 (4): 1–23CrossRefGoogle Scholar
  2. 2.
    Blair SN, Kohl III HW, Barlow CE, et al. Changes in physical fitness and all-cause mortality: a prospectivestudy of healthy and unhealthy men. JAMA 1995; 273: 1093–8PubMedCrossRefGoogle Scholar
  3. 3.
    Sun Q, Townsend MK, Okereke OI, et al. Physical activity at midlife in relation to successful survival inwomen at age 70 years or older. Arch Intern Med 2010; 170: 194–201PubMedCrossRefGoogle Scholar
  4. 4.
    Wolfe RR. The underappreciated role of muscle in health and disease. Am J Clin Nutr 2006; 84: 475–82PubMedGoogle Scholar
  5. 5.
    Cawthon PM, Fox KM, Gandra SR, et al. Do muscle mass, muscle density, strength, and physical function similarly influence risk of hospitalization in older adults? J Am Geriatr Soc 2009; 57: 1411–9PubMedCrossRefGoogle Scholar
  6. 6.
    Suetta C, Magnusson SP, Beyer N, et al. Effect of strength training on muscle function in elderly hospitalized patients. Scand J Med Sci Sports 2007; 17: 464–72PubMedCrossRefGoogle Scholar
  7. 7.
    Tanasescu M, Leitzmann MF, Rimm EB, et al. Exercise type and intensity in relation to coronary heart disease in men. 2002; 288 (16): 1994–2000Google Scholar
  8. 8.
    Kadar L, Albertsson M, Areberg J, et al. The prognostic value of body protein in patients with lung cancer. Ann NY Acad Sci 2000; 904: 584–91PubMedCrossRefGoogle Scholar
  9. 9.
    Anker SD, Steinborn W, Strassburg S. Cardiac cachexia. Ann Med 2004; 36: 518–29PubMedCrossRefGoogle Scholar
  10. 10.
    Metter EJ, Talbot LA, Schrager M, et al. Skeletal muscle strength as a predictor of all-cause mortality in healthymen. J Gerontol A Biol Sci Med Sci 2002; 57: B359–65PubMedCrossRefGoogle Scholar
  11. 11.
    Morley JE, Anker SD, Evans WJ. Cachexia and aging: an update based on the Fourth International Cachexia Meeting. J Nutr Health Aging 2009; 13: 47–55PubMedCrossRefGoogle Scholar
  12. 12.
    Phillips SM. Resistance exercise: good for more than just Grandma and Grandpa’smuscles. Appl Physiol Nutr Metab 2007; 32: 1198–205PubMedCrossRefGoogle Scholar
  13. 13.
    Hurley BF, Roth SM. Strength training in the elderly: effects on risk factors for age-related diseases. Sports Med 2000; 30: 249–68PubMedCrossRefGoogle Scholar
  14. 14.
    Braith RW, Stewart KJ. Resistance exercise training: its role in the prevention of cardiovascular disease. Circulation 2006; 113: 2642–50PubMedCrossRefGoogle Scholar
  15. 15.
    Pendergast DR, Fisher NM, Calkins E. Cardiovascular, neuromuscular, and metabolic alterations with age leadingto frailty. J Gerontol 1993; 48 (SpecNo): 61–7PubMedCrossRefGoogle Scholar
  16. 16.
    Evans WJ. Skeletal muscle loss: cachexia, sarcopenia, and inactivity. Am J Clin Nutr 2010; 91: 1123–7SCrossRefGoogle Scholar
  17. 17.
    Muller F. The nature and mechanism of superoxide production by the electron transport chain: its relevance toaging. J Am Aging Assoc 2000; 23: 227–53Google Scholar
  18. 18.
    Parise G, Kaczor JJ, Mahoney DJ, et al. Oxidative stress and the mitochondrial theory of aging in human skeletalmuscle. Exp Geront 2004; 39: 1391–400CrossRefGoogle Scholar
  19. 19.
    Melov S, Tarnopolsky MA, Beckman K, et al. Resistance exercise reverses aging in human skeletal muscle. PLo S One 2007; 2: (5) E465CrossRefGoogle Scholar
  20. 20.
    Li Y, Li HZ, Hu P, et al. Generation and bioenergetic analysis of cybrids containing mitochondrial DNA frommouse skeletal muscle during aging. Nucleic Acids Res 2010; 38 (6) 1913–21PubMedCrossRefGoogle Scholar
  21. 21.
    Parise G, Phillips SM, Kaczor JJ, et al. Antioxidant enzyme activity is up-regulated after unilateral resistance exercisetraining in older adults. Free Radic Biol Med 2005; 39: 289–95PubMedCrossRefGoogle Scholar
  22. 22.
    Parise G, Brose AN, Tarnopolsky MA. Resistance exercise training decreases oxidative damage to DNA and increasescytochrome oxidase activity in older adults. Exp Gerontol 2005; 40: 173–80PubMedCrossRefGoogle Scholar
  23. 23.
    Vincent KR, Vincent HK, Braith RW, et al. Resistance exercise training attenuates exercise-induced lipid peroxidationin the elderly. Eur J Appl Physiol 2002; 87: 416–23PubMedCrossRefGoogle Scholar
  24. 24.
    Kyriakouli DS, Boesch P, Taylor RW, et al. Progress and prospects: gene therapy for mitochondrial DNA disease. Gene Ther 2008; 15: 1017–23PubMedCrossRefGoogle Scholar
  25. 25.
    DiPenta JM, Green-Johnson JM, Murphy RJ. Type 2 diabetes mellitus, resistance training, and innate immunity:is there a common link? Appl Physiol Nutr Metab 2007; 32: 1025–35CrossRefGoogle Scholar
  26. 26.
    Murphy JL, Blakely EL, Schaefer AM, et al. Resistance training in patients with single, large-scale deletions ofmitochondrial DNA. Brain 2008; 131: 2832–40PubMedCrossRefGoogle Scholar
  27. 27.
    Johnston AP, De LM, Parise G. Resistance training, sarcopenia, and the mitochondrial theory of aging. Appl Physiol Nutr Metab 2008; 33: 191–9PubMedCrossRefGoogle Scholar
  28. 28.
    Petersen KF, Befroy D, Dufour S, et al. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 2003; 300: 1140–2PubMedCrossRefGoogle Scholar
  29. 29.
    Befroy DE, Petersen KF, Dufour S, et al. Impaired mitochondrial substrate oxidation in muscle of insulinresistantoffspring of type 2 diabetic patients. Diabetes 2007; 56: 1376–81PubMedCrossRefGoogle Scholar
  30. 30.
    Rotig A, Bonnefont JP, Munnich A. Mitochondrial diabetes mellitus. Diabetes Metab 1996; 22: 291–8PubMedGoogle Scholar
  31. 31.
    Grundy SM, Cleeman JI, Daniels SR, et al. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 2005; 112: 2735–52PubMedCrossRefGoogle Scholar
  32. 32.
    Alberti KG, Zimmet P, Shaw J. Metabolic syndrome: a new world-wide definition. A Consensus Statement fromthe International Diabetes Federation Diabet Med 2006; 23: 469–80Google Scholar
  33. 33.
    Reaven G. The metabolic syndrome or the insulin resistance syndrome? Different names, different concepts, anddifferent goals. Endocrinol Metab Clin North Am 2004; 33: 283–303PubMedCrossRefGoogle Scholar
  34. 34.
    Despres JP. Abdominal obesity and the metabolic syndrome. In: Bray G, Ryan D, editors. Overweight andmetabolic syndrome. New York: Springer, 2006: 137–52CrossRefGoogle Scholar
  35. 35.
    Libby P. Prevention and treatment of atherosclerosis. In: Kasper DL, Braunwald E, Fauci AS, et al., editors. Harrison’s principles of internal medicine. New York: McGraw-Hill, 2005: 1430–2Google Scholar
  36. 36.
    Jurca R, Lamonte MJ, Church TS, et al. Associations of muscle strength and fitness with metabolic syndrome inmen. Med Sci Sports Exerc 2004; 36: 1301–7PubMedCrossRefGoogle Scholar
  37. 37.
    Jurca R, Lamonte MJ, Barlow CE, et al. Association of muscular strength with incidence of metabolic syndromein men. Med Sci Sports Exerc 2005; 37: 1849–55PubMedCrossRefGoogle Scholar
  38. 38.
    Ruiz JR, Sui X, Lobelo F, et al. Muscular strength and adiposity as predictors of adulthood cancer mortality inmen. Cancer Epidemiol Biomarkers Prev 2009; 18: 1468–76PubMedCrossRefGoogle Scholar
  39. 39.
    Atlantis E, Martin SA, Haren MT, et al. Inverse associations between muscle mass, strength, and the metabolicsyndrome. Metabolism 2009; 58: 1013–22PubMedCrossRefGoogle Scholar
  40. 40.
    Rader DJ. Effect of insulin resistance, dyslipidemia, and intra-abdominal adiposity on the development of cardiovasculardisease and diabetes mellitus. Am J Med 2007; 120 (3): S12–8PubMedCrossRefGoogle Scholar
  41. 41.
    Powers AC. Diabetes mellitus. In: Kasper DL, Braunwald E, Fauci AS, et al., editors. Harrison’s principles of internal medicine. New York: McGraw-Hill, 2005: 2152–8Google Scholar
  42. 42.
    Ford ES, Giles WH, Dietz WH. Prevalence of the metabolic syndrome among US adults: findings from the thirdNational Health and Nutrition Examination Survey. JAMA 2002; 287: 356–9PubMedCrossRefGoogle Scholar
  43. 43.
    Narayan KM, Boyle JP, Thompson TJ, et al. Lifetime risk for diabetes mellitus in the United States. JAMA 2003; 290: 1884–90PubMedCrossRefGoogle Scholar
  44. 44.
    Colberg SR, Sigal RJ, Fernhall B, et al. Exercise and type 2 diabetes. The American College of Sports Medicine andthe American Diabetes Association joint position statementexecutive summary Diabetes Care 2010; 33: 2692–6Google Scholar
  45. 45.
    Selvin E, Steffes MW, Zhu H, et al. Glycated hemoglobin, diabetes, and cardiovascular risk in nondiabetic adults. N Engl J Med 2010; 362: 800–11PubMedCrossRefGoogle Scholar
  46. 46.
    Nathan D. International Expert Committee report on the role of the A1C assay in the diagnosis of diabetes. Diabetes Care 2009; 32: 1327–34CrossRefGoogle Scholar
  47. 47.
    Park SW, Goodpaster BH, Strotmeyer ES, et al. Decreased muscle strength and quality in older adults with type 2diabetes: the health, aging, and body composition study. Diabetes 2006; 55: 1813–8PubMedCrossRefGoogle Scholar
  48. 48.
    Park SW, Goodpaster BH, Strotmeyer ES, et al. Accelerated loss of skeletal muscle strength in older adultswith type 2 diabetes: the health, aging, and body compositionstudy. Diabetes Care 2007; 30: 1507–12PubMedCrossRefGoogle Scholar
  49. 49.
    Park SW, Goodpaster BH, Lee JS, et al. Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care 2009; 32: 1993–7PubMedCrossRefGoogle Scholar
  50. 50.
    Castaneda C, Layne JE, Munoz-Orians L, et al. A randomized controlled trial of resistance exercise training toimprove glycemic control in older adults with type 2 diabetes. Diabetes Care 2002; 25: 2335–41PubMedCrossRefGoogle Scholar
  51. 51.
    Khaw KT, Wareham N, Luben R, et al. Glycated haemoglobin, diabetes, and mortality in men in Norfolk cohortof European Prospective Investigation of Cancer and Nutrition(EPIC-Norfolk). BMJ 2001 Jun 1; 322 (7277): 1–6CrossRefGoogle Scholar
  52. 52.
    Manley S. Haemoglobin A1c — marker for complications of type 2 diabetes: the experience from the UK Prospective Diabetes Study (UKPDS). Clin Chem Lab Med 2003; 41: 1182–90PubMedCrossRefGoogle Scholar
  53. 53.
    Calles-Escandon J, Lovato LC, Simons-Morton DG, et al. Effect of intensive compared with standard glycemiatreatment strategies on mortality by baseline subgroupcharacteristics: the Action to Control Cardiovascular Riskin Diabetes (ACCORD) trial. Diabetes Care 2010; 33: 721–7PubMedCrossRefGoogle Scholar
  54. 54.
    Cauza E, Hanusch-Enserer U, Strasser B, et al. The relative benefits of endurance and strength training on the metabolicfactors and muscle function of people with type 2diabetes mellitus. Arch Phys Med Rehabil 2005; 86: 1527–33PubMedCrossRefGoogle Scholar
  55. 55.
    Brooks N, Layne JE, Gordon PL, et al. Strength training improves muscle quality and insulin sensitivity in Hispanicolder adults with type 2 diabetes. Int J Med Sci 2007; 4: 19–27CrossRefGoogle Scholar
  56. 56.
    Dunstan DW, Daly RM, Owen N, et al. High-intensity resistance training improves glycemic control in olderpatientswith type 2 diabetes. Diabetes Care 2002; 25: 1729–36PubMedCrossRefGoogle Scholar
  57. 57.
    Gordon PL, Vannier E, Hamada K, et al. Resistance training alters cytokine gene expression in skeletal muscleof adults with type 2 diabetes. Int J Immunopathol Pharmacol 2006; 19: 739–49PubMedGoogle Scholar
  58. 58.
    Baldi JC, Snowling N. Resistance training improves glycaemic control in obese type 2 diabetic men. Int J Sports Med 2003; 24: 419–23PubMedCrossRefGoogle Scholar
  59. 59.
    Snowling NJ, Hopkins WG. Effects of different modes of exercise training on glucose control and risk factors forcomplications in type 2 diabetic patients: a meta-analysis. Diabetes Care 2006; 29: 2518–27PubMedCrossRefGoogle Scholar
  60. 60.
    Balducci S, Alessi E, Cardelli P, et al. Effects of different modes of exercise training on glucose control and risk factors for complications in type 2 diabetic patients: ameta-analysis: response to Snowling and Hopkins [letter]. Diabetes Care 2007; 30: E25PubMedCrossRefGoogle Scholar
  61. 61.
    Sigal RJ, Kenny GP, Boule NG, et al. Effects of aerobic training, resistance training, or both on glycemic controlin type 2 diabetes: a randomized trial. Ann Intern Med 2007; 147: 357–69PubMedGoogle Scholar
  62. 62.
    Weeks DL. Exercise interventions for diabetes control: do we really know that strength training is better than endurancetraining? Arch Phys Med Rehabil 2007; 88: 397–8PubMedCrossRefGoogle Scholar
  63. 63.
    Bweir S, Al-Jarrah M, Almalty AM, et al. Resistance exercise training lowers HbA1c more than aerobic trainingin adults with type 2 diabetes. Diabetol Metab Syndr 2009; 1: 27PubMedCrossRefGoogle Scholar
  64. 64.
    Smutok MA, Reece C, Kokkinos PF, et al. Effects of exercise training modality on glucose tolerance in men withabnormal glucose regulation. Int J Sports Med 1994; 15: 283–9PubMedCrossRefGoogle Scholar
  65. 65.
    Miller JP, Pratley RE, Goldberg AP, et al. Strength training increases insulin action in healthy 50- to 65-yr-oldmen. J Appl Physiol 1994; 77: 1122–7PubMedGoogle Scholar
  66. 66.
    Misra A, Alappan NK, Vikram NK, et al. Effect of supervised progressive resistance-exercise training protocolon insulin sensitivity, glycemia, lipids, and body compositionin Asian Indians with type 2 diabetes. Diabetes Care 2008; 31: 1282–7PubMedCrossRefGoogle Scholar
  67. 67.
    Miller W, Sherman W, Ivy J. Effect of strength training on glucose tolerance and post-glucose insulin response. Med Sci Sports Exerc 1984; 16: 539–43PubMedGoogle Scholar
  68. 68.
    Close GL, Kayani A, Vasilaki A, et al. Skeletal muscle damage with exercise and aging. Sports Med 2005; 35: 413–27PubMedCrossRefGoogle Scholar
  69. 69.
    Ryan AS, Pratley RE, Goldberg AP, et al. Resistive training increases insulin action in postmenopausal women. J Gerontol A Biol Sci Med Sci 1996; 51: M199–205PubMedCrossRefGoogle Scholar
  70. 70.
    Ibanez J, Izquierdo M, Arguelles I, et al. Twice-weekly progressive resistance training decreases abdominal fatand improves insulin sensitivity in older men with type 2diabetes. Diabetes Care 2005; 28: 662–7PubMedCrossRefGoogle Scholar
  71. 71.
    Ryan AS, Hurlbut DE, Lott ME, et al. Insulin action after resistive training in insulin resistant older men andwomen. J Am Geriatr Soc 2001; 49: 247–53PubMedCrossRefGoogle Scholar
  72. 72.
    Ishii T, Yamakita T, Sato T, et al. Resistance training improves insulin sensitivity in NIDDM subjects withoutaltering maximal oxygen uptake. Diabetes Care 1998; 21: 1353–5PubMedCrossRefGoogle Scholar
  73. 73.
    Holten MK, Zacho M, Gaster M, et al. Strength training increases insulin-mediated glucose uptake, GLUT4 content,and insulin signaling in skeletal muscle in patientswith type 2 diabetes. Diabetes 2004; 53: 294–305PubMedCrossRefGoogle Scholar
  74. 74.
    Davidson LE, Hudson R, Kilpatrick K, et al. Effects of exercise modality on insulin resistance and functionallimitation in older adults: a randomized controlled trial. Arch Intern Med 2009; 169: 122–31PubMedCrossRefGoogle Scholar
  75. 75.
    Tresierras MA, Balady GJ. Resistance training in the treatment of diabetes and obesity: mechanisms and outcomes. J Cardiopulm Rehabil Prev 2009; 29: 67–75PubMedGoogle Scholar
  76. 76.
    Kuk JL, Kilpatrick K, Davidson LE, et al. Whole-body skeletal muscle mass is not related to glucose tolerance orinsulin sensitivity in overweight and obese men andwomen. Appl Physiol Nutr Metab 2008; 33: 769–74PubMedCrossRefGoogle Scholar
  77. 77.
    Klimcakova E, Polak J, Moro C, et al. Dynamic strength training improves insulin sensitivity without alteringplasma levels and gene expression of adipokines in subcutaneousadipose tissue in obese men. J Clin Endocrinol Metab 2006; 91: 5107–12PubMedCrossRefGoogle Scholar
  78. 78.
    Reynolds TH 4th, Supiano MA, Dengel DR. Resistance training enhances insulin-mediated glucose disposal withminimal effect on the tumor necrosis factor-alpha systemin older hypertensives. Metabolism 2004; 53: 397–402PubMedCrossRefGoogle Scholar
  79. 79.
    Smith Jr SC. Multiple risk factors for cardiovascular disease and diabetes mellitus. Am J Med 2007; 120: S3–11PubMedCrossRefGoogle Scholar
  80. 80.
    Li C, Ford ES, McGuire LC, et al. Increasing trends in waist circumference and abdominal obesity among USadults. Obesity (Silver Spring) 2007; 15: 216–24CrossRefGoogle Scholar
  81. 81.
    Treuth M, Hunter G, Kekes-szabo T, et al. Reduction in intra-abdominal adipose tissue after strength training inolder women. J Appl Physiol 1995; 78: 1425–31PubMedGoogle Scholar
  82. 82.
    Hunter GR, Bryan DR, Wetzstein CJ, et al. Resistance training and intra-abdominal adipose tissue in older menand women. Med Sci Sports Exerc 2002; 34: 1023–8PubMedCrossRefGoogle Scholar
  83. 83.
    Hunter GR, Brock DW, Byrne NM, et al. Exercise training prevents regain of visceral fat for 1 year following weightloss. Obesity (Silver Spring) 2010; 18 (4): 690–5CrossRefGoogle Scholar
  84. 84.
    Schmitz KH, Hannan PJ, Stovitz SD, et al. Strength training and adiposity in premenopausal women: strong, healthy,and empowered study. Am J Clin Nutr 2007; 86: 566–72PubMedGoogle Scholar
  85. 85.
    Borkan G, Hults D, Gerzof S, et al. Comparison of body composition in middle-aged and elderly males usingcomputed tomography. Am J Phy Anthropol 1984; 66: 289–95CrossRefGoogle Scholar
  86. 86.
    Taaffe DR, Henwood TR, Nalls MA, et al. Alterations in muscle attenuation following detraining and retraining inresistance-trained older adults. Gerontology 2009; 55: 217–23PubMedCrossRefGoogle Scholar
  87. 87.
    Dyck DJ, Bonen A. Muscle contraction increases palmitate esterification and oxidation and triacylglycerol oxidation. Am J Physiol 1998; 275: E888–96PubMedGoogle Scholar
  88. 88.
    Sacchetti M, Saltin B, Osada T, et al. Intramuscular fatty acid metabolism in contracting and non-contractinghuman skeletal muscle. J Physiol 2002; 540: 387–95PubMedCrossRefGoogle Scholar
  89. 89.
    Yao L, Delmonico MJ, Roth SM, et al. Adrenergic receptor genotype influence on midthigh intermuscular fatresponse to strength training in middle-aged and olderadults. J Gerontol A Biol Sci Med Sci 2007; 62: 658–63PubMedCrossRefGoogle Scholar
  90. 90.
    Pighon A, Paquette A, Barsalani R, et al. Substituting food restriction by resistance training prevents liver and bodyfat regain in ovariectomized rats. Climacteric 2009; 12: 153–64PubMedCrossRefGoogle Scholar
  91. 91.
    Kotronen A, Yki-Jarvinen H. Fatty liver: a novel component of the metabolic syndrome. Arterioscler Thromb Vasc Biol 2008; 28: 27–38PubMedCrossRefGoogle Scholar
  92. 92.
    Samuel VT, Liu ZX, Qu X, et al. Mechanism of hepatic insulin resistance in non-alcoholic fatty liver disease. J Biol Chem 2004; 279: 32345–53PubMedCrossRefGoogle Scholar
  93. 93.
    Pratley R, Nicklas B, Rubin M, et al. Strength training increases resting metabolic rate and norepinephrine levelsin healthy 50- to 65-yr-old men. J Appl Physiol 1994; 76: 133–7PubMedCrossRefGoogle Scholar
  94. 94.
    Lemmer JT, Ivey FM, Ryan AS, et al. Effect of strength training on resting metabolic rate and physical activity:age and gender comparisons. Med Sci Sports Exerc 2001; 33: 532–41PubMedGoogle Scholar
  95. 95.
    Hurley B, Seals D, Ehsani A, et al. Effects of high intensity strength training on cardiovascular function. Med Sci Sports Exerc 1984; 16: 483–8PubMedCrossRefGoogle Scholar
  96. 96.
    Lloyd-Jones D, Adams R, Carnethon M, et al. Heart disease and stroke statistics: 2009 update. A report from theAmerican Heart Association Statistics Committee andStroke Statistics Subcommittee Circulation 2009; 119: 480–6Google Scholar
  97. 97.
    Williams MA, Haskell WL, Ades PA, et al. Resistance exercise in individuals with and without cardiovasculardisease: 2007 update. A scientific statement from theAmerican Heart Association Council on Clinical Cardiologyand Council on Nutrition, Physical Activity, andMetabolism Circulation 2007; 116: 572–84Google Scholar
  98. 98.
    Kelley GA, Kelley KS. Impact of progressive resistance training on lipids and lipoproteins in adults: a meta-analysisof randomized controlled trials. Prev Med 2009; 48: 9–19PubMedCrossRefGoogle Scholar
  99. 99.
    Kelley GA, Kelley KS. Impact of progressive resistance training on lipids and lipoproteins in adults: another lookat a meta-analysis using prediction intervals. Prev Med 2009; 49: 473–5PubMedCrossRefGoogle Scholar
  100. 100.
    Fahlman MM, Boardley D, Lambert CP, et al. Effects of endurance training and resistance training on plasmalipoprotein profiles in elderly women. J Gerontol A Biol Sci Med Sci 2002; 57: B54–60PubMedCrossRefGoogle Scholar
  101. 101.
    Halverstadt A, Phares DA, Ferrell RE, et al. High-density lipoprotein-cholesterol, its subfractions, and responses toexercise training are dependent on endothelial lipase genotype. Metabolism 2003; 52: 1505–11PubMedCrossRefGoogle Scholar
  102. 102.
    Wilund KR, Ferrell RE, Phares DA, et al. Changes in highdensity lipoprotein-cholesterol subfractions with exercisetraining may be dependent on cholesteryl ester transferprotein (CETP) genotype. Metabolism 2002; 51: 774–8PubMedCrossRefGoogle Scholar
  103. 103.
    Chobanian AV, Bakris GL, Black HR, et al. The seventh report of the joint national committee on prevention, detection,evaluation, and treatment of high blood pressure:the JNC 7 report. JAMA 2003; 289: 2560–72PubMedCrossRefGoogle Scholar
  104. 104.
    Vasan RS, Larson MG, Leip EP, et al. Assessment of frequency of progression to hypertension in nonhypertensiveparticipants in the Framingham Heart Study:a cohort study. Lancet 2001; 358: 1682–6PubMedCrossRefGoogle Scholar
  105. 105.
    Kannel WB. Blood pressure as a cardiovascular risk factor: prevention and treatment. JAMA 1996; 275: 1571–6PubMedCrossRefGoogle Scholar
  106. 106.
    Cook NR, Cohen J, Hebert PR, et al. Implications of small reductions in diastolic blood pressure for primary prevention. Arch Intern Med 1995; 155: 701–9PubMedCrossRefGoogle Scholar
  107. 107.
    Martel GF, Hurlbut DE, Lott ME, et al. Strength training normalizes resting blood pressure in 65- to 73-year-oldmen and women with high normal blood pressure. J Am Geriatr Soc 1999; 47: 1215–21PubMedGoogle Scholar
  108. 108.
    Pescatello LS, Franklin BA, Fagard R, et al. American College of Sports Medicine position stand: exercise andhypertension. Med Sci Sports Exerc 2004; 36: 533–53PubMedCrossRefGoogle Scholar
  109. 109.
    Cornelissen VA, Fagard RH. Effect of resistance training on resting blood pressure: a meta-analysis of randomizedcontrolled trials. J Hypertens 2005; 23: 251–9PubMedCrossRefGoogle Scholar
  110. 110.
    Cononie CC, Graves J. Effect of exercise training on blood pressure in 70- to 79-yr-old men and women. Med Sci Sports and Exerc 1991; 23: 505–11Google Scholar
  111. 111.
    Smutok MA, Reece C, Kokkinos PF, et al. Aerobic versus strength training for risk factor intervention in middleagedmen at high risk for coronary heart disease. Metabolism 1993; 42: 177–84PubMedCrossRefGoogle Scholar
  112. 112.
    Lovell DI, Cuneo R, Gass GC. Resistance training reduces the blood pressure response of older men during submaximumaerobic exercise. Blood Press Monit 2009; 14: 137–44PubMedCrossRefGoogle Scholar
  113. 113.
    Maquet D, Croisier JL, Renard C, et al. Muscle performance in patients with fibromyalgia. Joint Bone Spine 2002; 69: 293–9PubMedCrossRefGoogle Scholar
  114. 114.
    Gilliland BC. Fibromyalgia, arthritis associated with systemic diseases and other arthritides. In: Kasper DL, Braunwald E, Fauci AS, et al., editors. Harrison’s principlesof internal medicine. New York: McGraw-Hill, 2005: 2055–6Google Scholar
  115. 115.
    Wolfe F, Ross K, Anderson J, et al. The prevalence and characteristics of fibromyalgia in the general population. Arthritis Rheum 1995; 38: 19–28PubMedCrossRefGoogle Scholar
  116. 116.
    Lowe JC, Yellin J, Honeyman-Lowe G. Female fibromyalgia patients: lower resting metabolic rates thanmatched healthycontrols. Med Sci Monit 2006; 12: CR282–9Google Scholar
  117. 117.
    Bennett R. Growth hormone in musculoskeletal pain states. Curr Pain Headache Rep 2005; 9: 331–8PubMedCrossRefGoogle Scholar
  118. 118.
    Jensen B, Wittrup IH, Bliddal H, et al. Bone mineral density in fibromyalgia patients: correlation to disease activity. Scand J Rheumatol 2003; 32: 146–50PubMedCrossRefGoogle Scholar
  119. 119.
    Triadafilopoulos G, Simms RW, Goldenberg DL. Bowel dysfunction in fibromyalgia syndrome. Dig Dis Sci 1991; 36: 59–64PubMedCrossRefGoogle Scholar
  120. 120.
    Jacobsen S, Gam A, Egsmose C, et al. Bone mass and turnover in fibromyalgia. J Rheumatol 1993; 20: 856–9PubMedGoogle Scholar
  121. 121.
    Brach JS, Simonsick EM, Kritchevsky S, et al. The association between physical function and lifestyle activityand exercise in the health, aging and body compositionstudy. J Am Geriatr Soc 2004; 52: 502–9PubMedCrossRefGoogle Scholar
  122. 122.
    Henriksson C, Gundmark I, Bengtsson A, et al. Living with fibromyalgia: consequences for everyday life. Clin J Pain 1992; 8: 138–44PubMedCrossRefGoogle Scholar
  123. 123.
    Roth SM, Ferrell RF, Hurley BF. Strength training for the prevention and treatment of sarcopenia. J Nutr Health Aging 2000; 4: 143–55PubMedGoogle Scholar
  124. 124.
    Lemmer JT, Hurlbut DE, Martel GF, et al. Age and gender responses to strength training and detraining. Med Sci Sports Exerc 2000; 32: 1505–12PubMedCrossRefGoogle Scholar
  125. 125.
    Marcinik E, Potts J, Schlabach G, et al. Effects of strength training on lactate threshold and endurance performance. Med Sci Sports Exerc 1991; 23: 739–43PubMedGoogle Scholar
  126. 126.
    Ades P, Ballor D, Ashikaga T, et al. Weight training improves walking endurance in healthy elderly persons. Ann Intern Med 1996; 124: 568–72PubMedGoogle Scholar
  127. 127.
    Nicklas BJ, Ryan AS, Trueth MS, et al. Anabolic hormone and IGF-1 responses to acute and chronic resistive trainingin men aged 55-70 years. Int J Sports Med 1995; 16: 445–50PubMedCrossRefGoogle Scholar
  128. 128.
    Ryan AS, Ivey FM, Hurlbut DE, et al. Regional bone mineral density after resistive training in young and oldermen and women. Scand J Med Sci Sports 2004; 14: 16–23PubMedCrossRefGoogle Scholar
  129. 129.
    Nelson ME, Fiatarone MA, Morganti CM, et al. Effects of high-intensity strength training on multiple risk factorsfor osteoporotic fractures: a randomized controlled trial. JAMA 1994; 272: 1909–14PubMedCrossRefGoogle Scholar
  130. 130.
    Koffler K, Menkes A, Redmond R, et al. Strength training accelerates gastrointestinal transit in middle-aged andolder men. Med Sci Sports Exerc 1992; 24: 415–9PubMedGoogle Scholar
  131. 131.
    Hurley B, Redmond R, Pratley R, et al. Effects of strength training on muscle hypertrophy andmuscle cell disruptionin older men. Int J Sports Med 1995; 16: 380–6CrossRefGoogle Scholar
  132. 132.
    Delmonico MJ, Kostek MC, Doldo NA, et al. Effects of moderate-velocity strength training on peak muscle powerand movement velocity: do women respond differentlythan men? J Appl Physiol 2005; 99: 1712–8PubMedCrossRefGoogle Scholar
  133. 133.
    Tracy BL, Ivey FM, Hurlbut D, et al. Muscle quality II: effects of strength training in 65-75 year old men andwomen. J Appl Physiol 1999; 86: 195–201PubMedGoogle Scholar
  134. 134.
    Ivey FM, Tracy BL, Lemmer JT, et al. Effects of strength training and detraining on muscle quality: age and gendercomparisons. J Gerontol a Biol Sci Med Sci 2000; 55 (3): B152–7PubMedCrossRefGoogle Scholar
  135. 135.
    Treuth MS, Ryan AS, Pratley RE, et al. Effects of strength training on total and regional body composition in oldermen. J Appl Physiol 1994; 77: 614–20PubMedGoogle Scholar
  136. 136.
    Hanson ED, Srivatsan SR, Agrawal S, et al. Does strength training improve function: strength, power, and body compositionrelationships. J Strength Cond Res 2009; 23: 2627–37PubMedCrossRefGoogle Scholar
  137. 137.
    Herman S, Kiely DK, Leveille S, et al. Upper and lower limb muscle power relationships in mobility-limited olderadults. J Gerontol A Biol Sci Med Sci 2005; 60: 476–80PubMedCrossRefGoogle Scholar
  138. 138.
    Mannerkorpi K. Exercise in fibromyalgia. Curr Opin Rheumatol 2005; 17: 190–4PubMedCrossRefGoogle Scholar
  139. 139.
    Jones KD, Burckhardt CS, Clark SR, et al. A randomized controlled trial of muscle strengthening versus flexibilitytraining in fibromyalgia. J Rheumatol 2002; 29: 1041–8PubMedGoogle Scholar
  140. 140.
    Kingsley JD, Panton LB, Toole T, et al. The effects of a 12-week strength-training program on strength and functionalityin women with fibromyalgia. Arch Phys Med Rehabil 2005; 86: 1713–21PubMedCrossRefGoogle Scholar
  141. 141.
    Valkeinen H, Hakkinen A, Hannonen P, et al. Acute heavy-resistance exercise-induced pain and neuromuscularfatigue in elderly women with fibromyalgia and inhealthy controls: effects of strength training. Arthritis Rheum 2006; 54: 1334–9PubMedCrossRefGoogle Scholar
  142. 142.
    Hakkinen A, Hakkinen K, Hannonen P, et al. Strength training induced adaptations in neuromuscular functionof premenopausal women with fibromyalgia: comparisonwith healthy women. Ann Rheum Dis 2001; 60: 21–6PubMedCrossRefGoogle Scholar
  143. 143.
    Valkeinen H, Hakkinen K, Pakarinen A, et al. Muscle hypertrophy, strength development, and serum hormonesduring strength training in elderly women with fibromyalgia. Scand J Rheumatol 2005; 34: 309–14PubMedCrossRefGoogle Scholar
  144. 144.
    Hakkinen K, Pakarinen A, Hannonen P, et al. Effects of strength training on muscle strength, cross-sectional area,maximal electromyographic activity, and serum hormonesin premenopausal women with fibromyalgia. J Rheumatol 2002; 29: 1287–95PubMedGoogle Scholar
  145. 145.
    Valkeinen H, Alen M, Hannonen P, et al. Changes in knee extension and flexion force, EMG and functional capacityduring strength training in older females with fibromyalgiaand healthy controls. Rheumatology (Oxford) 2004; 43: 225–8CrossRefGoogle Scholar
  146. 146.
    Bircan C, Karasel SA, Akgun B, et al. Effects of muscle strengthening versus aerobic exercise program in fibromyalgia. Rheumatol Int 2008; 28: 527–32PubMedCrossRefGoogle Scholar
  147. 147.
    Busch AJ, Schachter CL, Overend TJ, et al. Exercise for fibromyalgia: a systematic review. J Rheumatol 2008; 35: 1130–44PubMedGoogle Scholar
  148. 148.
    Brosseau L, Wells GA, Tugwell P, et al. Ottawa panel evidence-based clinical practice guidelines for strengtheningexercises in themanagement of fibromyalgia: part 2. Phys Ther 2008; 88: 873–86PubMedCrossRefGoogle Scholar
  149. 149.
    Lipsky PE. Rheumatoid arthritis. In: Kasper DL, Braunwald E, Fauci AS, et al., editors. Harrison’s principles of internal medicine. New York: McGraw-Hill, 2005: 1968–74Google Scholar
  150. 150.
    Iversen MD, Fossel AH, Daltroy LH. Rheumatologistpatient communication about exercise and physical therapyin the management of rheumatoid arthritis. Arthritis Care Res 1999; 12: 180–92PubMedCrossRefGoogle Scholar
  151. 151.
    Cairns AP, McVeigh JG. A systematic review of the effects of dynamic exercise in rheumatoid arthritis. Rheumatol Int. Epub 2009 Aug 22Google Scholar
  152. 152.
    Hakkinen A, Sokka T, Kotaniemi A, et al. Dynamic strength training in patients with early rheumatoid arthritisincreases muscle strength but not bone mineraldensity. J Rheumatol 1999; 26: 1257–63PubMedGoogle Scholar
  153. 153.
    Hakkinen A, Sokka T, Kotaniemi A, et al. A randomized two-year study of the effects of dynamic strength trainingon muscle strength, disease activity, functional capacity,and bone mineral density in early rheumatoid arthritis. Arthritis Rheum 2001; 44: 515–22PubMedCrossRefGoogle Scholar
  154. 154.
    Hakkinen A, Sokka T, Kautiainen H, et al. Sustained maintenance of exercise induced muscle strength gainsand normal bone mineral density in patients with earlyrheumatoid arthritis: a 5 year follow up. Ann Rheum Dis 2004; 63: 910–6PubMedCrossRefGoogle Scholar
  155. 155.
    McMeekin J, Stillman B, Story I, et al. The effects of knee extensor and flexor muscle training on the timed-up andgotest in individuals with rheumatoid arthritis. Physiother Res Int 1999; 4: 55–67Google Scholar
  156. 156.
    Flint-Wagner HG, Lisse J, Lohman TG, et al. Assessment of a sixteen-week training program on strength, pain, andfunction in rheumatoid arthritis patients. J Clin Rheumatol 2009; 15: 165–71PubMedCrossRefGoogle Scholar
  157. 157.
    Bird TD, Miller BL. Alzheimer’s disease and other dementias. In: Kasper DL, Braunwald E, Fauci AS, et al., editors. Harrison’s principles of internal medicine. New York: McGraw-Hill, 2005: 2393–8Google Scholar
  158. 158.
    Alzheimer’s Association. 2009 Alzheimer’s disease facts and figures. Alzheimers Dement 2009; 5: 234–70CrossRefGoogle Scholar
  159. 159.
    Alzheimer’s Association. 2010 Alzheimer’s disease facts and figures. Alzheimer’s Dement 2010 Mar; 6 (2): 158–94CrossRefGoogle Scholar
  160. 160.
    Buchman AS, Wilson RS, Bienias JL, et al. Change in body mass index and risk of incident Alzheimer disease. Neurology 2005; 65: 892–7PubMedCrossRefGoogle Scholar
  161. 161.
    Alfaro-Acha A, Al SS, Raji MA, et al. Handgrip strength and cognitive decline in older Mexican Americans. J Gerontol A Biol Sci Med Sci 2006; 61: 859–65PubMedCrossRefGoogle Scholar
  162. 162.
    Gustafson D, Rothenberg E, Blennow K, et al. An 18-year follow-up of overweight and risk of Alzheimer disease. Arch Intern Med 2003; 163: 1524–8PubMedCrossRefGoogle Scholar
  163. 163.
    Boyle PA, Buchman AS, Wilson RS, et al. Association of muscle strength with the risk of Alzheimer disease and therate of cognitive decline in community-dwelling olderpersons. Arch Neurol 2009; 66: 1339–44PubMedCrossRefGoogle Scholar
  164. 164.
    Buchman AS, Schneider JA, Leurgans S, et al. Physical frailty in older persons is associated with Alzheimer diseasepathology. Neurology 2008; 71: 499–504PubMedCrossRefGoogle Scholar
  165. 165.
    Lachman ME, Neupert SD, Bertrand R, et al. The effects of strength training on memory in older adults. J Aging Phys Act 2006; 14: 59–73PubMedGoogle Scholar
  166. 166.
    Cassilhas RC, Viana VA, Grassmann V, et al. The impact of resistance exercise on the cognitive function of the elderly. Med Sci Sports Exerc 2007; 39: 1401–7PubMedCrossRefGoogle Scholar
  167. 167.
    Liu-Ambrose T, Donaldson MG. Exercise and cognition in older adults: is there a role for resistance trainingprogrammes? Br J Sports Med 2009; 43: 25–7PubMedCrossRefGoogle Scholar
  168. 168.
    Liu-Ambrose T, Nagamatsu LS, Graf P, et al. Resistance training and executive functions: a 12-month randomizedcontrolled trial. Arch Intern Med 2010; 170: 170–8PubMedCrossRefGoogle Scholar
  169. 169.
    Davis JC, Marra CA, Beattie BL, et al. Sustained cognitive and economic benefits of resistance training amongcommunity-dwelling senior women: a 1-year follow-upstudy of the Brain Power study. Arch Intern Med 2010; 170: 2036–8PubMedCrossRefGoogle Scholar
  170. 170.
    Krogh J, Saltin B, Gluud C, et al. The DEMO trial:a randomized, parallel-group, observer-blinded clinicaltrial of strength versus aerobic versus relaxation trainingfor patients with mild to moderate depression. J Clin Psychiatry 2009; 70: 790–800PubMedCrossRefGoogle Scholar

Copyright information

© Adis Data Information BV 2011

Authors and Affiliations

  • Ben F. Hurley
    • 1
  • Erik D. Hanson
    • 1
  • Andrew K. Sheaff
    • 1
  1. 1.Department of Kinesiology, School of Public HealthUniversity of MarylandCollege ParkUSA

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