Skip to main content

Effects of Exercise Training on Chronic Inflammation in Obesity

Current Evidence and Potential Mechanisms

Abstract

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.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  Article  Google Scholar 

  12. 12.

    Petersen AM, Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol. 2005;98(4):1154–62.

    PubMed  CAS  Article  Google Scholar 

  13. 13.

    You T, Nicklas BJ. Effects of exercise on adipokines and the metabolic syndrome. Curr Diab Rep. 2008;8(1):7–11.

    PubMed  CAS  Article  Google 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.

    PubMed  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    Article  CAS  Google 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.

    PubMed  Article  Google 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.

    PubMed  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google Scholar 

  27. 27.

    Patel SR, Zhu X, Storfer-Isser A, et al. Sleep duration and biomarkers of inflammation. Sleep. 2009;32(2):200–4.

    PubMed  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  CAS  Article  Google Scholar 

  31. 31.

    Kershaw EE, Flier JS. Adipose tissue as an endocrine organ. J Clin Endocrinol Metab. 2004;89(6):2548–56.

    PubMed  CAS  Article  Google Scholar 

  32. 32.

    Libby P, Ridker PM, Maseri A. Inflammation and atherosclerosis. Circulation. 2002;105(9):1135–43.

    PubMed  CAS  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    Article  Google Scholar 

  46. 46.

    Paul M, Poyan Mehr A, Kreutz R. Physiology of local renin-angiotensin systems. Phys Rev. 2006;86(3):747–803.

    CAS  Article  Google 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.

    CAS  Article  Google 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.

    PubMed  CAS  Google 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.

    PubMed  CAS  Article  Google Scholar 

  50. 50.

    Avogaro A, de Kreutzenberg SV. Mechanisms of endothelial dysfunction in obesity. Clin Chim Acta. 2005;360(1–2):9–26.

    PubMed  CAS  Article  Google Scholar 

  51. 51.

    Libby P. Inflammation in atherosclerosis. Nature. 2002;420(6917):868–74.

    PubMed  CAS  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  CAS  Google Scholar 

  55. 55.

    McMurray RG, Hackney AC. Interactions of metabolic hormones, adipose tissue and exercise. Sports Medicine. 2005;35(5):393–412.

    PubMed  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  Google 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).

    PubMed  Article  Google 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.

    CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  Article  Google 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.

    CAS  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    CAS  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    CAS  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google Scholar 

  107. 107.

    Fischer CP. Interleukin-6 in acute exercise and training: what is the biological relevance? Exerc Immunol Rev. 2006;12:6–33.

    PubMed  Google Scholar 

  108. 108.

    Pedersen BK, Steensberg A, Schjerling P. Muscle-derived interleukin-6: possible biological effects. J Physiol. 2001;536(Pt 2):329–37.

    PubMed  CAS  Article  Google Scholar 

  109. 109.

    Abeywardena MY, Leifert WR, Warnes KE, et al. Cardiovascular biology of interleukin-6. Curr Pharm Des. 2009;15(15):1809–21.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Google 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].

  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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google Scholar 

  134. 134.

    Frenette PS, Wagner DD. Adhesion molecules: part 1. N Engl J Med. 1996;334(23):1526–9.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google Scholar 

  150. 150.

    Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu Rev Immunol. 2003;21:335–76.

    PubMed  CAS  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  CAS  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Tongjian You.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

You, T., Arsenis, N.C., Disanzo, B.L. et al. Effects of Exercise Training on Chronic Inflammation in Obesity. Sports Med 43, 243–256 (2013). https://doi.org/10.1007/s40279-013-0023-3

Download citation

Keywords

  • Vascular Endothelial Growth Factor
  • Adipose Tissue
  • Exercise Training
  • Resistance Exercise
  • Obese Individual