Effects of exercise training on chronic inflammation in obesity: Current evidence and potential mechanisms

Sports Medicine

Volumn 43, Issue 4, 2013, Pages 243-256

  You, Tongjian ^a   Arsenis, Nicole C ^a   Disanzo, Beth L ^b   Lamonte, Michael J ^b  

^a UNIVERSITY OF MASSACHUSETTS BOSTON   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE;

ADIPOSE TISSUE; CHRONIC DISEASE; EXERCISE; HUMAN; IMMUNOLOGY; INFLAMMATION; OBESITY; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; WEIGHT REDUCTION;

ADIPOSE TISSUE; CHRONIC DISEASE; CYTOKINES; EXERCISE; HUMANS; INFLAMMATION; OBESITY; WEIGHT LOSS;

EID: 84876555951     PISSN: 01121642     EISSN: 11792035     Source Type: Journal    
DOI: 10.1007/s40279-013-0023-3     Document Type: Review

References (160)

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.
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.
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.
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.
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.
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.
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.
8. Roytblat L, Rachinsky M, Fisher A, et al. Raised interleukin-6 levels in obese patients. Obes Res. 2000;8(9):673-5.
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.
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.
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.
12. Petersen AM, Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol. 2005;98(4):1154-62.
13. You T, Nicklas BJ. Effects of exercise on adipokines and the metabolic syndrome. Curr Diab Rep. 2008;8(1):7-11.
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.
15. Beavers KM, Brinkley TE, Nicklas BJ. Effect of exercise training on chronic inflammation. Clin Chim Acta. 2010;411(11-12):785-93.
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.
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.
18. Kumar V, Abbas AK, Fausto N. Robbins and Cotran pathologic basis of disease. 7th ed. Philadelphia: Elsevier Saunders; 2005.
19. Libby P. Inflammatory mechanisms: the molecular basis of inflammation and disease. Nutr Rev. 2007;65(12 Pt 2):S140-6.
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.
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.
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.
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.
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.
25. Walter RE, Wilk JB, Larson MG, et al. Systemic inflammation and COPD: the Framingham heart study. Chest. 2008;133(1):19-25.
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.
27. Patel SR, Zhu X, Storfer-Isser A, et al. Sleep duration and biomarkers of inflammation. Sleep. 2009;32(2):200-4.
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.
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.
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.
31. Kershaw EE, Flier JS. Adipose tissue as an endocrine organ. J Clin Endocrinol Metab. 2004;89(6):2548-56.
32. Libby P, Ridker PM, Maseri A. Inflammation and atherosclerosis. Circulation. 2002;105(9):1135-43.
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.
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.
35. Ye J. Emerging role of adipose tissue hypoxia in obesity and insulin resistance. Int J Obes (Lond). 2009;33(1):54-66.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
46. Paul M, Poyan Mehr A, Kreutz R. Physiology of local renin-angiotensin systems. Phys Rev. 2006;86(3):747-803.
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.
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.
49. Caballero AE. Endothelial dysfunction in obesity and insulin resistance: a road to diabetes and heart disease. Obes Res. 2003;11(11):1278-89.
50. Avogaro A, de Kreutzenberg SV. Mechanisms of endothelial dysfunction in obesity. Clin Chim Acta. 2005;360(1-2):9-26.
51. Libby P. Inflammation in atherosclerosis. Nature. 2002;420(6917):868-74.
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.
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.
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.
55. McMurray RG, Hackney AC. Interactions of metabolic hormones, adipose tissue and exercise. Sports Medicine. 2005;35(5):393-412.
56. Albert MA, Glynn RJ, Ridker PM. Effect of physical activity on serum C-reactive protein. Am J Cardiol. 2004;93(2):221-5.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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).
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
107. Fischer CP. Interleukin-6 in acute exercise and training: what is the biological relevance? Exerc Immunol Rev. 2006;12:6-33.
108. Pedersen BK, Steensberg A, Schjerling P. Muscle-derived interleukin-6: possible biological effects. J Physiol. 2001;536(Pt 2):329-37.
109. Abeywardena MY, Leifert WR, Warnes KE, et al. Cardiovascular biology of interleukin-6. Curr Pharm Des. 2009;15(15):1809-21.
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.
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.
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.
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.
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.
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. 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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
134. Frenette PS, Wagner DD. Adhesion molecules: part 1. N Engl J Med. 1996;334(23):1526-9.
135. Bevilacqua MP, Nelson RM, Mannori G, et al. Endothelial-leukocyte adhesion molecules in human disease. Annu Rev Med. 1994;45:361-78.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
150. Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu Rev Immunol. 2003;21:335-76.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.