Sports Medicine

, Volume 43, Issue 4, pp 243–256 | Cite as

Effects of Exercise Training on Chronic Inflammation in Obesity

Current Evidence and Potential Mechanisms
  • Tongjian YouEmail author
  • Nicole C. Arsenis
  • Beth L. Disanzo
  • Michael J. LaMonte
Review Article


Chronic, systemic inflammation is an independent risk factor for several major clinical diseases. In obesity, circulating levels of inflammatory markers are elevated, possibly due to increased production of pro-inflammatory cytokines from several tissues/cells, including macrophages within adipose tissue, vascular endothelial cells and peripheral blood mononuclear cells. Recent evidence supports that adipose tissue hypoxia may be an important mechanism through which enlarged adipose tissue elicits local tissue inflammation and further contributes to systemic inflammation. Current evidence supports that exercise training, such as aerobic and resistance exercise, reduces chronic inflammation, especially in obese individuals with high levels of inflammatory biomarkers undergoing a longer-term intervention. Several studies have reported that this effect is independent of the exercise-induced weight loss. There are several mechanisms through which exercise training reduces chronic inflammation, including its effect on muscle tissue to generate muscle-derived, anti-inflammatory ‘myokine’, its effect on adipose tissue to improve hypoxia and reduce local adipose tissue inflammation, its effect on endothelial cells to reduce leukocyte adhesion and cytokine production systemically, and its effect on the immune system to lower the number of pro-inflammatory cells and reduce pro-inflammatory cytokine production per cell. Of these potential mechanisms, the effect of exercise training on adipose tissue oxygenation is worth further investigation, as it is very likely that exercise training stimulates adipose tissue angiogenesis and increases blood flow, thereby reducing hypoxia and the associated chronic inflammation in adipose tissue of obese individuals.


Vascular Endothelial Growth Factor Adipose Tissue Exercise Training Resistance Exercise Obese Individual 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors have no conflicts of interest to declare that are directly relevant to the content of this review. No funding was used to assist in the preparation of this review.


  1. 1.
    Ridker PM, Hennekens CH, Buring JE, et al. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med. 2000;342(12):836–43.PubMedCrossRefGoogle Scholar
  2. 2.
    Ridker PM, Rifai N, Stampfer MJ, et al. Plasma concentration of interleukin-6 and the risk of future myocardial infarction among apparently healthy men. Circulation. 2000;101(15):1767–72.PubMedCrossRefGoogle Scholar
  3. 3.
    Ridker PM, Rifai N, Pfeffer M, et al. Elevation of tumor necrosis factor-alpha and increased risk of recurrent coronary events after myocardial infarction. Circulation. 2000;101(18):2149–53.PubMedCrossRefGoogle Scholar
  4. 4.
    Wilson PW, Nam BH, Pencina M, et al. C-reactive protein and risk of cardiovascular disease in men and women from the Framingham Heart Study. Arch Intern Med. 2005;165(21):2473–8.PubMedCrossRefGoogle Scholar
  5. 5.
    Festa A, D’Agostino R Jr, Tracy RP, et al. Elevated levels of acute-phase proteins and plasminogen activator inhibitor-1 predict the development of type 2 diabetes: the insulin resistance atherosclerosis study. Diabetes. 2002;51(4):1131–7.PubMedCrossRefGoogle Scholar
  6. 6.
    Laaksonen DE, Niskanen L, Nyyssonen K, et al. C-reactive protein and the development of the metabolic syndrome and diabetes in middle-aged men. Diabetologia. 2004;47(8):1403–10.PubMedCrossRefGoogle Scholar
  7. 7.
    Visser M, Bouter LM, McQuillan GM, et al. Elevated C-reactive protein levels in overweight and obese adults. JAMA. 1999;282(22):2131–5.PubMedCrossRefGoogle Scholar
  8. 8.
    Roytblat L, Rachinsky M, Fisher A, et al. Raised interleukin-6 levels in obese patients. Obes Res. 2000;8(9):673–5.PubMedCrossRefGoogle Scholar
  9. 9.
    Mohamed-Ali V, Goodrick S, Bulmer K, et al. Production of soluble tumor necrosis factor receptors by human subcutaneous adipose tissue in vivo. Am J Physiol. 1999;277(6 Pt 1):E971–5.PubMedGoogle Scholar
  10. 10.
    Olszanecka-Glinianowicz M, Zahorska-Markiewicz B, Janowska J, et al. Serum concentrations of nitric oxide, tumor necrosis factor (TNF)-alpha and TNF soluble receptors in women with overweight and obesity. Metabolism. 2004;53(10):1268–73.PubMedCrossRefGoogle Scholar
  11. 11.
    Nicklas BJ, You T, Pahor M. Behavioural treatments for chronic systemic inflammation: effects of dietary weight loss and exercise training. CMAJ. 2005;172(9):1199–209.PubMedCrossRefGoogle Scholar
  12. 12.
    Petersen AM, Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol. 2005;98(4):1154–62.PubMedCrossRefGoogle Scholar
  13. 13.
    You T, Nicklas BJ. Effects of exercise on adipokines and the metabolic syndrome. Curr Diab Rep. 2008;8(1):7–11.PubMedCrossRefGoogle Scholar
  14. 14.
    Nicklas BJ, Brinkley TE. Exercise training as a treatment for chronic inflammation in the elderly. Exerc Sport Sci Rev. 2009;37(4):165–70.PubMedGoogle Scholar
  15. 15.
    Beavers KM, Brinkley TE, Nicklas BJ. Effect of exercise training on chronic inflammation. Clin Chim Acta. 2010;411(11–12):785–93.PubMedCrossRefGoogle Scholar
  16. 16.
    Gleeson M, Bishop NC, Stensel DJ, et al. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol. 2011;11(9):607–15.PubMedCrossRefGoogle Scholar
  17. 17.
    Lavie CJ, Church TS, Milani RV, et al. Impact of physical activity, cardiorespiratory fitness, and exercise training on markers of inflammation. J Cardiopulm Rehabil Prev. 2011;31(3):137–45.PubMedGoogle Scholar
  18. 18.
    Kumar V, Abbas AK, Fausto N. Robbins and Cotran pathologic basis of disease. 7th ed. Philadelphia: Elsevier Saunders; 2005.Google Scholar
  19. 19.
    Libby P. Inflammatory mechanisms: the molecular basis of inflammation and disease. Nutr Rev. 2007;65(12 Pt 2):S140–6.PubMedCrossRefGoogle Scholar
  20. 20.
    Slade GD, Ghezzi EM, Heiss G, et al. Relationship between periodontal disease and C-reactive protein among adults in the Atherosclerosis Risk in Communities study. Arch Intern Med. 2003;163(10):1172–9.PubMedCrossRefGoogle Scholar
  21. 21.
    Ding C, Parameswaran V, Udayan R, et al. Circulating levels of inflammatory markers predict change in bone mineral density and resorption in older adults: a longitudinal study. J Clin Endocrinol Metab. 2008;93(5):1952–8.PubMedCrossRefGoogle Scholar
  22. 22.
    Schaap LA, Pluijm SM, Deeg DJ, et al. Inflammatory markers and loss of muscle mass (sarcopenia) and strength. Am J Med. 2006;119(6):526e9–17.CrossRefGoogle Scholar
  23. 23.
    dos Santos Silva I, De Stavola BL, Pizzi C, et al. Circulating levels of coagulation and inflammation markers and cancer risks: individual participant analysis of data from three long-term cohorts. Int J Epidemiol. 2010;39(3):699–709.PubMedCrossRefGoogle Scholar
  24. 24.
    Penninx BW, Abbas H, Ambrosius W, et al. Inflammatory markers and physical function among older adults with knee osteoarthritis. J Rheumatol. 2004;31(10):2027–31.PubMedGoogle Scholar
  25. 25.
    Walter RE, Wilk JB, Larson MG, et al. Systemic inflammation and COPD: the Framingham heart study. Chest. 2008;133(1):19–25.PubMedCrossRefGoogle Scholar
  26. 26.
    Seddon JM, Gensler G, Milton RC, et al. Association between C-reactive protein and age-related macular degeneration. JAMA. 2004;291(6):704–10.PubMedCrossRefGoogle Scholar
  27. 27.
    Patel SR, Zhu X, Storfer-Isser A, et al. Sleep duration and biomarkers of inflammation. Sleep. 2009;32(2):200–4.PubMedGoogle Scholar
  28. 28.
    Penninx BW, Kritchevsky SB, Yaffe K, et al. Inflammatory markers and depressed mood in older persons: results from the health, aging and body composition study. Biol Psychiatry. 2003;54(5):566–72.PubMedCrossRefGoogle Scholar
  29. 29.
    Engelhart MJ, Geerlings MI, Meijer J, et al. Inflammatory proteins in plasma and the risk of dementia: the Rotterdam study. Arch Neurol. 2004;61(5):668–72.PubMedCrossRefGoogle Scholar
  30. 30.
    Yoneda M, Mawatari H, Fujita K, et al. High-sensitivity C-reactive protein is an independent clinical feature of nonalcoholic steatohepatitis (NASH) and also of the severity of fibrosis in NASH. J Gastroenterol. 2007;42(7):573–82.PubMedCrossRefGoogle Scholar
  31. 31.
    Kershaw EE, Flier JS. Adipose tissue as an endocrine organ. J Clin Endocrinol Metab. 2004;89(6):2548–56.PubMedCrossRefGoogle Scholar
  32. 32.
    Libby P, Ridker PM, Maseri A. Inflammation and atherosclerosis. Circulation. 2002;105(9):1135–43.PubMedCrossRefGoogle Scholar
  33. 33.
    Ribeiro F, Alves AJ, Duarte JA, et al. Is exercise training an effective therapy targeting endothelial dysfunction and vascular wall inflammation? Int J Cardiol. 2010;141(3):214–21.PubMedCrossRefGoogle Scholar
  34. 34.
    Ghanim H, Aljada A, Hofmeyer D, et al. Circulating mononuclear cells in the obese are in a proinflammatory state. Circulation. 2004;110(12):1564–71.PubMedCrossRefGoogle Scholar
  35. 35.
    Ye J. Emerging role of adipose tissue hypoxia in obesity and insulin resistance. Int J Obes (Lond). 2009;33(1):54–66.CrossRefGoogle Scholar
  36. 36.
    Hosogai N, Fukuhara A, Oshima K, et al. Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes. 2007;56(4):901–11.PubMedCrossRefGoogle Scholar
  37. 37.
    Ye J, Gao Z, Yin J, et al. Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. Am J Physiol Endocrinol Metab. 2007;293(4):E1118–28.PubMedCrossRefGoogle Scholar
  38. 38.
    Rausch ME, Weisberg S, Vardhana P, et al. Obesity in C57BL/6J mice is characterized by adipose tissue hypoxia and cytotoxic T-cell infiltration. Int J Obes (Lond). 2008;32(3):451–63.CrossRefGoogle Scholar
  39. 39.
    Pasarica M, Sereda OR, Redman LM, et al. Reduced adipose tissue oxygenation in human obesity: evidence for rarefaction, macrophage chemotaxis, and inflammation without an angiogenic response. Diabetes. 2009;58(3):718–25.PubMedCrossRefGoogle Scholar
  40. 40.
    Goossens GH, Bizzarri A, Venteclef N, et al. Increased adipose tissue oxygen tension in obese compared with lean men is accompanied by insulin resistance, impaired adipose tissue capillarization, and inflammation. Circulation. 2011;124(1):67–76.PubMedCrossRefGoogle Scholar
  41. 41.
    Ferri C, Desideri G, Valenti M, et al. Early upregulation of endothelial adhesion molecules in obese hypertensive men. Hypertension. 1999;34(4 Pt 1):568–73.PubMedCrossRefGoogle Scholar
  42. 42.
    Spencer M, Unal R, Zhu B, et al. Adipose tissue extracellular matrix and vascular abnormalities in obesity and insulin resistance. J Clin Endocrinol Metab. 2011;96(12):E1990–8.PubMedCrossRefGoogle Scholar
  43. 43.
    Elias I, Franckhauser S, Ferre T, et al. Adipose tissue overexpression of vascular endothelial growth factor protects against diet-induced obesity and insulin resistance. Diabetes. 2012;61:1801–13.PubMedCrossRefGoogle Scholar
  44. 44.
    Michailidou Z, Turban S, Miller E, et al. Increased angiogenesis protects against adipose hypoxia and fibrosis in metabolic disease-resistant 11beta-hydroxysteroid dehydrogenase type 1 (HSD1)-deficient mice. J Biol Chem. 2012;287(6):4188–97.PubMedCrossRefGoogle Scholar
  45. 45.
    Sivitz WI, Wayson SM, Bayless ML, et al. Obesity impairs vascular relaxation in human subjects: hyperglycemia exaggerates adrenergic vasoconstriction arterial dysfunction in obesity and diabetes. J Diabetes Comp. 2007;21(3):149–57.CrossRefGoogle Scholar
  46. 46.
    Paul M, Poyan Mehr A, Kreutz R. Physiology of local renin-angiotensin systems. Phys Rev. 2006;86(3):747–803.CrossRefGoogle Scholar
  47. 47.
    Boustany CM, Bharadwaj K, Daugherty A, et al. Activation of the systemic and adipose renin-angiotensin system in rats with diet-induced obesity and hypertension. Am J Physiol Regy Int Comp Physiol. 2004;287(4):R943–9.CrossRefGoogle Scholar
  48. 48.
    West DB, Prinz WA, Francendese AA, et al. Adipocyte blood flow is decreased in obese Zucker rats. Am J Physiol. 1987;253(2 Pt 2):R228–33.PubMedGoogle Scholar
  49. 49.
    Caballero AE. Endothelial dysfunction in obesity and insulin resistance: a road to diabetes and heart disease. Obes Res. 2003;11(11):1278–89.PubMedCrossRefGoogle Scholar
  50. 50.
    Avogaro A, de Kreutzenberg SV. Mechanisms of endothelial dysfunction in obesity. Clin Chim Acta. 2005;360(1–2):9–26.PubMedCrossRefGoogle Scholar
  51. 51.
    Libby P. Inflammation in atherosclerosis. Nature. 2002;420(6917):868–74.PubMedCrossRefGoogle Scholar
  52. 52.
    Klein S, Burke LE, Bray GA, et al. Clinical implications of obesity with specific focus on cardiovascular disease: a statement for professionals from the American Heart Association Council on Nutrition, Physical Activity, and Metabolism: endorsed by the American College of Cardiology Foundation. Circulation. 2004;110(18):2952–67.PubMedCrossRefGoogle Scholar
  53. 53.
    Donnelly JE, Blair SN, Jakicic JM, et al. American College of Sports Medicine Position Stand. Appropriate physical activity intervention strategies for weight loss and prevention of weight regain for adults. Med Sci Sports Exerc. 2009;41(2):459–71.PubMedCrossRefGoogle Scholar
  54. 54.
    Jakicic JM, Otto AD. Physical activity considerations for the treatment and prevention of obesity. Am J Clin Nutr. 2005;82(1 Suppl):226S–9S.PubMedGoogle Scholar
  55. 55.
    McMurray RG, Hackney AC. Interactions of metabolic hormones, adipose tissue and exercise. Sports Medicine. 2005;35(5):393–412.PubMedCrossRefGoogle Scholar
  56. 56.
    Albert MA, Glynn RJ, Ridker PM. Effect of physical activity on serum C-reactive protein. Am J Cardiol. 2004;93(2):221–5.PubMedCrossRefGoogle Scholar
  57. 57.
    Aronson D, Sella R, Sheikh-Ahmad M, et al. The association between cardiorespiratory fitness and C-reactive protein in subjects with the metabolic syndrome. J Am Coll Cardiol. 2004;44(10):2003–7.PubMedCrossRefGoogle Scholar
  58. 58.
    Aronson D, Sheikh-Ahmad M, Avizohar O, et al. C-reactive protein is inversely related to physical fitness in middle-aged subjects. Atherosclerosis. 2004;176(1):173–9.PubMedCrossRefGoogle Scholar
  59. 59.
    Borodulin K, Laatikainen T, Salomaa V, et al. Associations of leisure time physical activity, self-rated physical fitness, and estimated aerobic fitness with serum C-reactive protein among 3,803 adults. Atherosclerosis. 2006;185(2):381–7.PubMedCrossRefGoogle Scholar
  60. 60.
    Church TS, Barlow CE, Earnest CP, et al. Associations between cardiorespiratory fitness and C-reactive protein in men. Arterioscler Thromb Vasc Biol. 2002;22(11):1869–76.PubMedCrossRefGoogle Scholar
  61. 61.
    Geffken DF, Cushman M, Burke GL, et al. Association between physical activity and markers of inflammation in a healthy elderly population. Am J Epidemiol. 2001;153(3):242–50.PubMedCrossRefGoogle Scholar
  62. 62.
    LaMonte MJ, Durstine JL, Yanowitz FG, et al. Cardiorespiratory fitness and C-reactive protein among a tri-ethnic sample of women. Circulation. 2002;106(4):403–6.PubMedCrossRefGoogle Scholar
  63. 63.
    McGavock JM, Mandic S, Vonder Muhll I, et al. Low cardiorespiratory fitness is associated with elevated C-reactive protein levels in women with type 2 diabetes. Diabetes Care. 2004;27(2):320–5.PubMedCrossRefGoogle Scholar
  64. 64.
    Mora S, Lee IM, Buring JE, et al. Association of physical activity and body mass index with novel and traditional cardiovascular biomarkers in women. JAMA. 2006;295(12):1412–9.PubMedCrossRefGoogle Scholar
  65. 65.
    Pischon T, Hankinson SE, Hotamisligil GS, et al. Leisure-time physical activity and reduced plasma levels of obesity-related inflammatory markers. Obes Res. 2003;11(9):1055–64.PubMedCrossRefGoogle Scholar
  66. 66.
    Stauffer BL, Hoetzer GL, Smith DT, et al. Plasma C-reactive protein is not elevated in physically active postmenopausal women taking hormone replacement therapy. J Appl Physiol. 2004;96(1):143–8.PubMedCrossRefGoogle Scholar
  67. 67.
    Wannamethee SG, Lowe GD, Whincup PH, et al. Physical activity and hemostatic and inflammatory variables in elderly men. Circulation. 2002;105(15):1785–90.PubMedCrossRefGoogle Scholar
  68. 68.
    Williams MJ, Milne BJ, Hancox RJ, et al. C-reactive protein and cardiorespiratory fitness in young adults. Eur J Cardiovasc Prev Rehabil. 2005;12(3):216–20.PubMedCrossRefGoogle Scholar
  69. 69.
    Hjelstuen A, Anderssen SA, Holme I, et al. Markers of inflammation are inversely related to physical activity and fitness in sedentary men with treated hypertension. Am J Hypertens. 2006;19(7):669–75. (discussion 76–77).PubMedCrossRefGoogle Scholar
  70. 70.
    Ruiz JR, Ortega FB, Warnberg J, et al. Associations of low-grade inflammation with physical activity, fitness and fatness in prepubertal children; the European Youth Heart study. Int J Obes (Lond). 2007;31(10):1545–51.CrossRefGoogle Scholar
  71. 71.
    Hamer M, Steptoe A. Walking, vigorous physical activity, and markers of hemostasis and inflammation in healthy men and women. Scand J Med Sci Sports. 2008;18(6):736–41.PubMedCrossRefGoogle Scholar
  72. 72.
    Majka DS, Chang RW, Vu TH, et al. Physical activity and high-sensitivity C-reactive protein: the multi-ethnic study of atherosclerosis. Am J Prev Med. 2009;36(1):56–62.PubMedCrossRefGoogle Scholar
  73. 73.
    Autenrieth C, Schneider A, Doring A, et al. Association between different domains of physical activity and markers of inflammation. Med Sci Sports Exerc. 2009;41(9):1706–13.PubMedCrossRefGoogle Scholar
  74. 74.
    Sabiston CM, Castonguay A, Low NC, et al. Vigorous physical activity and low-grade systemic inflammation in adolescent boys and girls. Int J Pediatr Obes. 2010;5(6):509–15.PubMedCrossRefGoogle Scholar
  75. 75.
    Lavoie ME, Rabasa-Lhoret R, Doucet E, et al. Association between physical activity energy expenditure and inflammatory markers in sedentary overweight and obese women. Int J Obes (Lond). 2010;34(9):1387–95.CrossRefGoogle Scholar
  76. 76.
    Bergstrom G, Behre CJ, Schmidt C. Moderate intensities of leisure-time physical activity are associated with lower levels of high-sensitivity C-reactive protein in healthy middle-aged men. Angiology. 2011;63:412–5.PubMedCrossRefGoogle Scholar
  77. 77.
    Jennersjo P, Ludvigsson J, Lanne T, et al. Pedometer-determined physical activity is linked to low systemic inflammation and low arterial stiffness in Type 2 diabetes. Diabet Med. 2012;29:1119–25.PubMedCrossRefGoogle Scholar
  78. 78.
    Lee IM, Sesso HD, Ridker PM, et al. Physical activity and inflammation in a multiethnic cohort of women. Med Sci Sports Exerc. 2012;44(6):1088–96.PubMedCrossRefGoogle Scholar
  79. 79.
    Mora S, Cook N, Buring JE, et al. Physical activity and reduced risk of cardiovascular events: potential mediating mechanisms. Circulation. 2007;116(19):2110–8.PubMedCrossRefGoogle Scholar
  80. 80.
    Manns PJ, Williams DP, Snow CM, et al. Physical activity, body fat, and serum C-reactive protein in postmenopausal women with and without hormone replacement. Am J Hum Biol. 2003;15(1):91–100.PubMedCrossRefGoogle Scholar
  81. 81.
    Rawson ES, Freedson PS, Osganian SK, et al. Body mass index, but not physical activity, is associated with C-reactive protein. Med Sci Sports Exerc. 2003;35(7):1160–6.PubMedCrossRefGoogle Scholar
  82. 82.
    Taaffe DR, Villa ML, Holloway L, et al. Bone mineral density in older non-Hispanic Caucasian and Mexican-American women: relationship to lean and fat mass. Ann Hum Biol. 2000;27(4):331–44.PubMedCrossRefGoogle Scholar
  83. 83.
    Verdaet D, Dendale P, De Bacquer D, et al. Association between leisure time physical activity and markers of chronic inflammation related to coronary heart disease. Atherosclerosis. 2004;176(2):303–10.PubMedCrossRefGoogle Scholar
  84. 84.
    Kohut ML, McCann DA, Russell DW, et al. Aerobic exercise, but not flexibility/resistance exercise, reduces serum IL-18, CRP, and IL-6 independent of beta-blockers, BMI, and psychosocial factors in older adults. Brain Behav Immun. 2006;20(3):201–9.PubMedCrossRefGoogle Scholar
  85. 85.
    Olson TP, Dengel DR, Leon AS, et al. Changes in inflammatory biomarkers following one-year of moderate resistance training in overweight women. Int J Obes (Lond). 2007;31(6):996–1003.CrossRefGoogle Scholar
  86. 86.
    Nicklas BJ, Hsu FC, Brinkley TJ, et al. Exercise training and plasma C-reactive protein and interleukin-6 in elderly people. J Am Geriatr Soc. 2008;56(11):2045–52.PubMedCrossRefGoogle Scholar
  87. 87.
    Campbell KL, Campbell PT, Ulrich CM, et al. No reduction in C-reactive protein following a 12-month randomized controlled trial of exercise in men and women. Cancer Epidemiol Biomarkers Prev. 2008;17(7):1714–8.PubMedCrossRefGoogle Scholar
  88. 88.
    Campbell PT, Campbell KL, Wener MH, et al. A yearlong exercise intervention decreases CRP among obese postmenopausal women. Med Sci Sports Exerc. 2009;41(8):1533–9.PubMedCrossRefGoogle Scholar
  89. 89.
    Church TS, Earnest CP, Thompson AM, et al. Exercise without weight loss does not reduce C-reactive protein: the INFLAME study. Med Sci Sports Exerc. 2010;42(4):708–16.PubMedCrossRefGoogle Scholar
  90. 90.
    Donges CE, Duffield R, Drinkwater EJ. Effects of resistance or aerobic exercise training on interleukin-6, C-reactive protein, and body composition. Med Sci Sports Exerc. 2010;42(2):304–13.PubMedCrossRefGoogle Scholar
  91. 91.
    Arikawa AY, Thomas W, Schmitz KH, et al. Sixteen weeks of exercise reduces C-reactive protein levels in young women. Med Sci Sports Exerc. 2011;43(6):1002–9.PubMedCrossRefGoogle Scholar
  92. 92.
    Nicklas BJ, Ambrosius W, Messier SP, et al. Diet-induced weight loss, exercise, and chronic inflammation in older, obese adults: a randomized controlled clinical trial. Am J Clin Nutr. 2004;79(4):544–51.PubMedGoogle Scholar
  93. 93.
    Fairey AS, Courneya KS, Field CJ, et al. Effect of exercise training on C-reactive protein in postmenopausal breast cancer survivors: a randomized controlled trial. Brain Behav Immun. 2005;19(5):381–8.PubMedCrossRefGoogle Scholar
  94. 94.
    Marcell TJ, McAuley KA, Traustadottir T, et al. Exercise training is not associated with improved levels of C-reactive protein or adiponectin. Metabolism. 2005;54(4):533–41.PubMedCrossRefGoogle Scholar
  95. 95.
    Brooks N, Layne JE, Gordon PL, et al. Strength training improves muscle quality and insulin sensitivity in Hispanic older adults with type 2 diabetes. Int J Med Sci. 2007;4(1):19–27.CrossRefGoogle Scholar
  96. 96.
    Kadoglou NP, Iliadis F, Angelopoulou N, et al. The anti-inflammatory effects of exercise training in patients with type 2 diabetes mellitus. Eur J Cardiovasc Prev Rehabil. 2007;14(6):837–43.PubMedCrossRefGoogle Scholar
  97. 97.
    Walther C, Mobius-Winkler S, Linke A, et al. Regular exercise training compared with percutaneous intervention leads to a reduction of inflammatory markers and cardiovascular events in patients with coronary artery disease. Eur J Cardiovasc Prev Rehabil. 2008;15(1):107–12.PubMedCrossRefGoogle Scholar
  98. 98.
    Stewart LK, Earnest CP, Blair SN, et al. Effects of different doses of physical activity on C-reactive protein among women. Med Sci Sports Exerc. 2010;42(4):701–7.PubMedCrossRefGoogle Scholar
  99. 99.
    Balducci S, Zanuso S, Nicolucci A, et al. Anti-inflammatory effect of exercise training in subjects with type 2 diabetes and the metabolic syndrome is dependent on exercise modalities and independent of weight loss. Nutr Metab Cardiovasc Dis. 2010;20(8):608–17.PubMedCrossRefGoogle Scholar
  100. 100.
    Martins RA, Neves AP, Coelho-Silva MJ, et al. The effect of aerobic versus strength-based training on high-sensitivity C-reactive protein in older adults. Eur J Appl Physiol. 2010;110(1):161–9.PubMedCrossRefGoogle Scholar
  101. 101.
    Jorge ML, de Oliveira VN, Resende NM, et al. The effects of aerobic, resistance, and combined exercise on metabolic control, inflammatory markers, adipocytokines, and muscle insulin signaling in patients with type 2 diabetes mellitus. Metabolism. 2011;60(9):1244–52.PubMedCrossRefGoogle Scholar
  102. 102.
    Swift DL, Johannsen NM, Earnest CP, et al. Effect of exercise training modality on C-reactive protein in type-2 diabetes. Med Sci Sports Exerc. 2011;44:1208–34.Google Scholar
  103. 103.
    Kadoglou NP, Fotiadis G, Athanasiadou Z, et al. The effects of resistance training on ApoB/ApoA-I ratio, Lp(a) and inflammatory markers in patients with type 2 diabetes. Endocrine. 2012;42:561–9.PubMedCrossRefGoogle Scholar
  104. 104.
    Balducci S, Zanuso S, Cardelli P, et al. Changes in physical fitness predict improvements in modifiable cardiovascular risk factors independently of body weight loss in subjects with type 2 diabetes participating in the Italian diabetes and exercise study (IDES). Diabetes Care. 2012;35:1347–54.PubMedCrossRefGoogle Scholar
  105. 105.
    Balducci S, Zanuso S, Cardelli P, et al. Supervised exercise training counterbalances the adverse effects of insulin therapy in overweight/obese subjects with type 2 diabetes. Diabetes Care. 2012;35(1):39–41.PubMedCrossRefGoogle Scholar
  106. 106.
    You T, Berman DM, Ryan AS, et al. Effects of hypocaloric diet and exercise training on inflammation and adipocyte lipolysis in obese postmenopausal women. J Clin Endocrinol Metab. 2004;89(4):1739–46.PubMedCrossRefGoogle Scholar
  107. 107.
    Fischer CP. Interleukin-6 in acute exercise and training: what is the biological relevance? Exerc Immunol Rev. 2006;12:6–33.PubMedGoogle Scholar
  108. 108.
    Pedersen BK, Steensberg A, Schjerling P. Muscle-derived interleukin-6: possible biological effects. J Physiol. 2001;536(Pt 2):329–37.PubMedCrossRefGoogle Scholar
  109. 109.
    Abeywardena MY, Leifert WR, Warnes KE, et al. Cardiovascular biology of interleukin-6. Curr Pharm Des. 2009;15(15):1809–21.PubMedCrossRefGoogle Scholar
  110. 110.
    Lyngso D, Simonsen L, Bulow J. Interleukin-6 production in human subcutaneous abdominal adipose tissue: the effect of exercise. J Physiol. 2002;543(Pt 1):373–8.PubMedCrossRefGoogle Scholar
  111. 111.
    Keller C, Keller P, Marshal S, et al. IL-6 gene expression in human adipose tissue in response to exercise–effect of carbohydrate ingestion. J Physiol. 2003;550(Pt 3):927–31.PubMedCrossRefGoogle Scholar
  112. 112.
    Connolly PH, Caiozzo VJ, Zaldivar F, et al. Effects of exercise on gene expression in human peripheral blood mononuclear cells. J Appl Physiol. 2004;97(4):1461–9.PubMedCrossRefGoogle Scholar
  113. 113.
    Haahr PM, Pedersen BK, Fomsgaard A, et al. Effect of physical exercise on in vitro production of interleukin 1, interleukin 6, tumour necrosis factor-alpha, interleukin 2 and interferon-gamma. Int J Sports Med. 1991;12(2):223–7.PubMedCrossRefGoogle Scholar
  114. 114.
    Moldoveanu AI, Shephard RJ, Shek PN. Exercise elevates plasma levels but not gene expression of IL-1beta, IL-6, and TNF-alpha in blood mononuclear cells. J Appl Physiol. 2000;89(4):1499–504.PubMedGoogle Scholar
  115. 115.
    Bernecker C, Scherr J, Schinner S, et al. Evidence for an exercise induced increase of TNF-alpha and IL-6 in marathon runners. Scand J Med Sci Sports. 2011 [Epub ahead of print].Google Scholar
  116. 116.
    Zoppini G, Targher G, Zamboni C, et al. Effects of moderate-intensity exercise training on plasma biomarkers of inflammation and endothelial dysfunction in older patients with type 2 diabetes. Nutr Metab Cardiovasc Dis. 2006;16(8):543–9.PubMedCrossRefGoogle Scholar
  117. 117.
    Polak J, Klimcakova E, Moro C, et al. Effect of aerobic training on plasma levels and subcutaneous abdominal adipose tissue gene expression of adiponectin, leptin, interleukin 6, and tumor necrosis factor alpha in obese women. Metabolism. 2006;55(10):1375–81.PubMedCrossRefGoogle Scholar
  118. 118.
    Klimcakova E, Polak J, Moro C, et al. Dynamic strength training improves insulin sensitivity without altering plasma levels and gene expression of adipokines in subcutaneous adipose tissue in obese men. J Clin Endocrinol Metab. 2006;91(12):5107–12.PubMedCrossRefGoogle Scholar
  119. 119.
    Leick L, Lindegaard B, Stensvold D, et al. Adipose tissue interleukin-18 mRNA and plasma interleukin-18: effect of obesity and exercise. Obesity (Silver Spring). 2007;15(2):356–63.CrossRefGoogle Scholar
  120. 120.
    Christiansen T, Paulsen SK, Bruun JM, et al. Exercise training versus diet-induced weight-loss on metabolic risk factors and inflammatory markers in obese subjects: a 12-week randomized intervention study. Am J Physiol Endocrinol Metab. 2010;298(4):E824–31.PubMedCrossRefGoogle Scholar
  121. 121.
    Gomez-Merino D, Drogou C, Guezennec CY, et al. Effects of chronic exercise on cytokine production in white adipose tissue and skeletal muscle of rats. Cytokine. 2007;40(1):23–9.PubMedCrossRefGoogle Scholar
  122. 122.
    Lira FS, Rosa JC, Yamashita AS, et al. Endurance training induces depot-specific changes in IL-10/TNF-alpha ratio in rat adipose tissue. Cytokine. 2009;45(2):80–5.PubMedCrossRefGoogle Scholar
  123. 123.
    Bradley RL, Jeon JY, Liu FF, et al. Voluntary exercise improves insulin sensitivity and adipose tissue inflammation in diet-induced obese mice. Am J Physiol Endocrinol Metab. 2008;295(3):E586–94.PubMedCrossRefGoogle Scholar
  124. 124.
    Vieira VJ, Valentine RJ, Wilund KR, et al. Effects of diet and exercise on metabolic disturbances in high-fat diet-fed mice. Cytokine. 2009;46(3):339–45.PubMedCrossRefGoogle Scholar
  125. 125.
    Vieira VJ, Valentine RJ, Wilund KR, et al. Effects of exercise and low-fat diet on adipose tissue inflammation and metabolic complications in obese mice. Am J Physiol Endocrinol Metab. 2009;296(5):E1164–71.PubMedCrossRefGoogle Scholar
  126. 126.
    Hatano D, Ogasawara J, Endoh S, et al. Effect of exercise training on the density of endothelial cells in the white adipose tissue of rats. Scand J Med Sci Sports. 2011;21(6):e115–21.PubMedCrossRefGoogle Scholar
  127. 127.
    Czarkowska-Paczek B, Zendzian-Piotrowska M, Bartlomiejczyk I, et al. The influence of physical exercise on the generation of TGF-beta1, PDGF-AA, and VEGF-A in adipose tissue. Eur J Appl Physiol. 2011;111(5):875–81.PubMedCrossRefGoogle Scholar
  128. 128.
    Frisbee JC, Samora JB, Peterson J, et al. Exercise training blunts microvascular rarefaction in the metabolic syndrome. Am J Physiol Heart Circ Physiol. 2006;291(5):H2483–92.PubMedCrossRefGoogle Scholar
  129. 129.
    Felix JV, Michelini LC. Training-induced pressure fall in spontaneously hypertensive rats is associated with reduced angiotensinogen mRNA expression within the nucleus tractus solitarii. Hypertension. 2007;50(4):780–5.PubMedCrossRefGoogle Scholar
  130. 130.
    Pereira MG, Ferreira JC, Bueno CR Jr, et al. Exercise training reduces cardiac angiotensin II levels and prevents cardiac dysfunction in a genetic model of sympathetic hyperactivity-induced heart failure in mice. Eur J Appl Physiol. 2009;105(6):843–50.PubMedCrossRefGoogle Scholar
  131. 131.
    Enevoldsen LH, Stallknecht B, Fluckey JD, et al. Effect of exercise training on in vivo lipolysis in intra-abdominal adipose tissue in rats. Am J Physiol Endocrinol Metab. 2000;279(3):E585–92.PubMedGoogle Scholar
  132. 132.
    Schmidt W, Maassen N, Trost F, et al. Training induced effects on blood volume, erythrocyte turnover and haemoglobin oxygen binding properties. Eur J Appl Physiol Occup Physiol. 1988;57(4):490–8.PubMedCrossRefGoogle Scholar
  133. 133.
    Heinicke K, Wolfarth B, Winchenbach P, et al. Blood volume and hemoglobin mass in elite athletes of different disciplines. Int J Sports Med. 2001;22(7):504–12.PubMedCrossRefGoogle Scholar
  134. 134.
    Frenette PS, Wagner DD. Adhesion molecules: part 1. N Engl J Med. 1996;334(23):1526–9.PubMedCrossRefGoogle Scholar
  135. 135.
    Bevilacqua MP, Nelson RM, Mannori G, et al. Endothelial-leukocyte adhesion molecules in human disease. Annu Rev Med. 1994;45:361–78.PubMedCrossRefGoogle Scholar
  136. 136.
    Wahl P, Bloch W, Schmidt A. Exercise has a positive effect on endothelial progenitor cells, which could be necessary for vascular adaptation processes. Int J Sports Med. 2007;28(5):374–80.PubMedCrossRefGoogle Scholar
  137. 137.
    Laufs U, Werner N, Link A, et al. Physical training increases endothelial progenitor cells, inhibits neointima formation, and enhances angiogenesis. Circulation. 2004;109(2):220–6.PubMedCrossRefGoogle Scholar
  138. 138.
    Sarto P, Balducci E, Balconi G, et al. Effects of exercise training on endothelial progenitor cells in patients with chronic heart failure. J Card Fail. 2007;13(9):701–8.PubMedCrossRefGoogle Scholar
  139. 139.
    Schlager O, Giurgea A, Schuhfried O, et al. Exercise training increases endothelial progenitor cells and decreases asymmetric dimethylarginine in peripheral arterial disease: a randomized controlled trial. Atherosclerosis. 2011;217(1):240–8.PubMedCrossRefGoogle Scholar
  140. 140.
    Steiner S, Niessner A, Ziegler S, et al. Endurance training increases the number of endothelial progenitor cells in patients with cardiovascular risk and coronary artery disease. Atherosclerosis. 2005;181(2):305–10.PubMedCrossRefGoogle Scholar
  141. 141.
    Schmidt-Lucke C, Reinhold D, Ansorge S, et al. Changes of plasma concentrations of soluble vascular cell adhesion molecule-1 and vascular endothelial growth factor after increased perfusion of lower extremities in humans. Endothelium. 2003;10(3):159–65.PubMedCrossRefGoogle Scholar
  142. 142.
    Di Francescomarino S, Sciartilli A, Di Valerio V, et al. The effect of physical exercise on endothelial function. Sports Med. 2009;39(10):797–812.PubMedCrossRefGoogle Scholar
  143. 143.
    Wegge JK, Roberts CK, Ngo TH, et al. Effect of diet and exercise intervention on inflammatory and adhesion molecules in postmenopausal women on hormone replacement therapy and at risk for coronary artery disease. Metabolism. 2004;53(3):377–81.PubMedCrossRefGoogle Scholar
  144. 144.
    Adamopoulos S, Parissis J, Kroupis C, et al. Physical training reduces peripheral markers of inflammation in patients with chronic heart failure. Eur Heart J. 2001;22(9):791–7.PubMedCrossRefGoogle Scholar
  145. 145.
    Bjornstad HH, Bruvik J, Bjornstad AB, et al. Exercise training decreases plasma levels of soluble CD40 ligand and P-selectin in patients with chronic heart failure. Eur J Cardiovasc Prev Rehabil. 2008;15(1):43–8.PubMedCrossRefGoogle Scholar
  146. 146.
    Yang AL, Chen HI. Chronic exercise reduces adhesion molecules/iNOS expression and partially reverses vascular responsiveness in hypercholesterolemic rabbit aortae. Atherosclerosis. 2003;169(1):11–7.PubMedCrossRefGoogle Scholar
  147. 147.
    Yang AL, Jen CJ, Chen HI. Effects of high-cholesterol diet and parallel exercise training on the vascular function of rabbit aortas: a time course study. J Appl Physiol. 2003;95(3):1194–200.PubMedGoogle Scholar
  148. 148.
    Sengenes C, Miranville A, Lolmede K, et al. The role of endothelial cells in inflamed adipose tissue. J Intern Med. 2007;262(4):415–21.PubMedCrossRefGoogle Scholar
  149. 149.
    Smith JK, Dykes R, Douglas JE, et al. Long-term exercise and atherogenic activity of blood mononuclear cells in persons at risk of developing ischemic heart disease. JAMA. 1999;281(18):1722–7.PubMedCrossRefGoogle Scholar
  150. 150.
    Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu Rev Immunol. 2003;21:335–76.PubMedCrossRefGoogle Scholar
  151. 151.
    McFarlin BK, Flynn MG, Campbell WW, et al. Physical activity status, but not age, influences inflammatory biomarkers and toll-like receptor 4. J Gerontol A Biol Sci Med Sci. 2006;61(4):388–93.PubMedCrossRefGoogle Scholar
  152. 152.
    Stewart LK, Flynn MG, Campbell WW, et al. Influence of exercise training and age on CD14+ cell-surface expression of toll-like receptor 2 and 4. Brain Behav Immun. 2005;19(5):389–97.PubMedCrossRefGoogle Scholar
  153. 153.
    Flynn MG, McFarlin BK, Phillips MD, et al. Toll-like receptor 4 and CD14 mRNA expression are lower in resistive exercise-trained elderly women. J Appl Physiol. 2003;95(5):1833–42.PubMedGoogle Scholar
  154. 154.
    McFarlin BK, Flynn MG, Campbell WW, et al. TLR4 is lower in resistance-trained older women and related to inflammatory cytokines. Med Sci Sports Exerc. 2004;36(11):1876–83.PubMedCrossRefGoogle Scholar
  155. 155.
    Belge KU, Dayyani F, Horelt A, et al. The proinflammatory CD14+CD16+DR++ monocytes are a major source of TNF. J Immunol. 2002;168(7):3536–42.PubMedGoogle Scholar
  156. 156.
    Timmerman KL, Flynn MG, Coen PM, et al. Exercise training-induced lowering of inflammatory (CD14+CD16+) monocytes: a role in the anti-inflammatory influence of exercise? J Leukoc Biol. 2008;84(5):1271–8.PubMedCrossRefGoogle Scholar
  157. 157.
    Coen PM, Flynn MG, Markofski MM, et al. Adding exercise to rosuvastatin treatment: influence on C-reactive protein, monocyte toll-like receptor 4 expression, and inflammatory monocyte (CD14+CD16+) population. Metabolism. 2010;59(12):1775–83.PubMedCrossRefGoogle Scholar
  158. 158.
    Yeh SH, Chuang H, Lin LW, et al. Regular tai chi chuan exercise enhances functional mobility and CD4CD25 regulatory T cells. Br J Sports Med. 2006;40(3):239–43.PubMedCrossRefGoogle Scholar
  159. 159.
    Yeh SH, Chuang H, Lin LW, et al. Tai chi chuan exercise decreases A1C levels along with increase of regulatory T-cells and decrease of cytotoxic T-cell population in type 2 diabetic patients. Diabetes Care. 2007;30(3):716–8.PubMedCrossRefGoogle Scholar
  160. 160.
    Yeh SH, Chuang H, Lin LW, et al. Regular Tai Chi Chuan exercise improves T cell helper function of patients with type 2 diabetes mellitus with an increase in T-bet transcription factor and IL-12 production. Br J Sports Med. 2009;43(11):845–50.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2013

Authors and Affiliations

  • Tongjian You
    • 1
    Email author
  • Nicole C. Arsenis
    • 2
  • Beth L. Disanzo
    • 3
  • Michael J. LaMonte
    • 4
  1. 1.Department of Exercise and Health Sciences, College of Nursing and Health SciencesUniversity of Massachusetts BostonBostonUSA
  2. 2.Department of Nursing, College of Nursing and Health SciencesUniversity of Massachusetts BostonBostonUSA
  3. 3.Department of Exercise and Nutrition Sciences, School of Public Health and Health ProfessionsState University of New York at BuffaloBuffaloUSA
  4. 4.Department of Social and Preventive Medicine, School of Public Health and Health ProfessionsState University of New York at BuffaloBuffaloUSA

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