Exercise-induced changes in inflammatory processes: Implications for thrombogenesis in cardiovascular disease

Annals of Medicine

Volumn 46, Issue 7, 2014, Pages 439-455

  Chen, Yu Wen ^a   Apostolakis, Stavros ^a   Lip, Gregory Y H ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Erythrocyte aggregability; Exercise; Inflammation; Leukocyte activation; Thrombosis

Indexed keywords

ADIPONECTIN; CD40 LIGAND; C REACTIVE PROTEIN; INTERLEUKIN 6;

BLOOD CLOTTING; CELL INTERACTION; ERYTHROCYTE; EXERCISE INTENSITY; FLOW KINETICS; HUMAN; LEUKOCYTE; LONG TERM EXPOSURE; METABOLIC EQUIVALENT; PHYSICAL ACTIVITY; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; THROMBOCYTE; VASCULITIS; BLOOD; CARDIOVASCULAR DISEASES; EXERCISE; FIBRINOLYSIS; INFLAMMATION; MEMBRANE MICROPARTICLE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; RESISTANCE TRAINING; SEDENTARY LIFESTYLE; THROMBOSIS;

ADIPONECTIN; BLOOD COAGULATION; BLOOD PLATELETS; C-REACTIVE PROTEIN; CARDIOVASCULAR DISEASES; CD40 LIGAND; CELL-DERIVED MICROPARTICLES; ERYTHROCYTES; EXERCISE; FIBRINOLYSIS; HUMANS; INFLAMMATION; INTERLEUKIN-6; LEUKOCYTES; RESISTANCE TRAINING; SEDENTARY LIFESTYLE; THROMBOSIS;

EID: 84909989687     PISSN: 07853890     EISSN: 13652060     Source Type: Journal    
DOI: 10.3109/07853890.2014.927713     Document Type: Review

References (145)

1. Pedersen BK. Body mass index-independent effect of fitness and physical activity for all-cause mortality. Scand J Med Sci Sports. 2007;17:196-204.
2. Myers J, Kaykha A, George S, Abella J, Zaheer N, Lear S, et al. Fitness versus physical activity patterns in predicting mortality in men. Am J Med. 2004;117:912-18.
3. Pedersen BK. The diseasome of physical inactivity - and the role of myokines in muscle - fat cross talk. J Physiol. 2009;587:5559-68.
4. Tuomilehto J, Lindstrom J, Eriksson JG, Valle TT, Hämäläinen H, Ilanne-Parikka P, et al.; Finnish Diabetes Prevention Study Group. Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N Engl J Med. 2001;344:1343-50.
5. Nocon M, Hiemann T, Muller-Riemenschneider F, Thalau F, Roll S, Willich SN. Association of physical activity with all-cause and cardiovascular mortality: a systematic review and meta-analysis. Eur J Cardiovasc Prev Rehabil. 2008;15:239-46.
6. Libby P, Okamoto Y, Rocha VZ, Folco E. Inflammation in atherosclerosis: transition from theory to practice. Circ J. 2010;74:213-20.
7. Shebuski RJ, Kilgore KS. Role of inflammatory mediators in thrombogenesis. J Pharmacol Exp Ther. 2002;300:729-35.
8. Santos MJ, Pedro LM, Canhão H, Fernandes E, Fernandes J, Canas da Silva J, et al. Hemorheological parameters are related to subclinical atherosclerosis in systemic lupus erythematosus and rheumatoid arthritis patients. Atherosclerosis. 2011;219:821-6.
9. Tzoulaki I, Murray GD, Lee AJ, Rumley A, Lowe GD, Fowkes FG. Relative value of inflammatory, hemostatic, and rheological factors for incident myocardial infarction and stroke: The Edinburgh Artery Study. Circulation. 2007;115:2119-27.
10. ten Cate JW, van der Poll T, Levi M, ten Cate H, van Deventer SJ. Cytokines: triggers of clinical thrombotic disease. Thromb Haemost. 1997;78:415-19.
11. Neumann FJ, Ott I, Marx N, Luther T, Kenngott S, Gawaz M, et al. Effect of human recombinant interleukin-6 and interleukin-8 on monocyte procoagulant activity. Arterioscler Thromb Vasc Biol. 1997;17:3399-405.
12. Cermak J, Key NS, Bach RR, Balla J, Jacob HS, Vercellotti GM. C-reactive protein induces human peripheral blood monocytes to synthesize tissue factor. Blood. 1993;82:513-20.
13. Burstein SA. Cytokines, platelet production and hemostasis. Platelets. 1997;8:93-104.
14. Amrani DL. Regulation of fibrinogen biosynthesis: glucocorticoid and interleukin-6 control. Blood Coagul Fibrinolysis. 1990;1:443-6.
15. Chirinos JA, Heresi GA, Velasquez H, Jy W, Jimenez JJ, Ahn E, et al. Elevation of endothelial microparticles, platelets, and leukocyte activation in patients with venous thromboembolism. J Am Coll Cardiol. 2005;45:1467-71.
16. Baskurt OK, Meiselman HJ. Activated polymorphonuclear leukocytes affect red blood cell aggregability. J Leukoc Biol. 1998;63:89-93.
17. Chu AJ. Role of tissue factor in thrombosis. Coagulation-inflammation-thrombosis circuit. Front Biosci. 2006;11:256-71.
18. Wakefield TW, Henke PK. The role of inflammation in early and late venous thrombosis: are there clinical implications? Semin Vasc Surg. 2005;18:118-29.
19. Blair SN, Kohl HW III, Barlow CE, Paffenbarger RS Jr, Gibbons LW, Macera CA. Changes in physical fitness and all-cause mortality. A prospective study of healthy and unhealthy men. JAMA. 1995;273:1093-8.
20. Kushi LH, Fee RM, Folsom AR, Mink PJ, Anderson KE, Sellers TA. Physical activity and mortality in postmenopausal women. JAMA. 1997;277:1287-92.
21. Tanasescu M, Leitzmann MF, Rimm EB, Willett WC, Stampfer MJ, Hu FB. Exercise type and intensity in relation to coronary heart disease in men. JAMA. 2002;288:1994-2000.
22. Dorn J, Naughton J, Imamura D, Trevisan M. Results of a multicenter randomized clinical trial of exercise and long-term survival in myocardial infarction patients: the National Exercise and Heart Disease Project (NEHDP). Circulation. 1999;100:1764-9.
23. Kokkinos P, Myers J, Kokkinos JP, Pittaras A, Narayan P, Manolis A, et al. Exercise capacity and mortality in black and white men. Circulation. 2008;117:614-22.
24. Myers J, Prakash M, Froelicher V, Do D, Partington S, Atwood JE. Exercise capacity and mortality among men referred for exercise testing. N Engl J Med. 2002;346:793-801.
25. Lee IM, Skerrett PJ. Physical activity and all-cause mortality: what is the dose-response relation? Med Sci Sports Exerc. 2001;33:S459-71.
26. Mora S, Cook N, Buring JE, Ridker PM, Lee IM. Physical activity and reduced risk of cardiovascular events: potential mediating mechanisms. Circulation. 2007;116:2110-18.
27. Panagiotakos DB, Pitsavos C, Chrysohoou C, Kavouras S, Stefanadis C. The associations between leisure-time physical activity and inflammatory and coagulation markers related to cardiovascular disease: the ATTICA Study. Prev Med. 2005;40:432-7.
28. Harris RA, Padilla J, Hanlon KP, Rink LD, Wallace JP. The flow-mediated dilation response to acute exercise in overweight active and inactive men. Obesity (Silver Spring). 2008;16:578-84.
29. Palmer-Kazen U, Religa P, Wahlberg E. Exercise in patients with intermittent claudication elicits signs of inflammation and angiogenesis. Eur J Vasc Endovasc Surg. 2009;38:689-96.
30. Andersson J, Jansson JH, Hellsten G, Nilsson TK, Hallmans G, Boman K. Effects of heavy endurance physical exercise on inflammatory markers in non-athletes. Atherosclerosis. 2010;209:601-5.
31. Markovitch D, Tyrrell RM, Thompson D. Acute moderate-intensity exercise in middle-aged men has neither an anti-nor proinflammatory effect. J Appl Physiol. 2008;105:260-5.
32. Mendham AE, Coutts AJ, Duffield R. The acute effects of aerobic exercise and modified rugby on inflammation and glucose homeostasis within Indigenous Australians. Eur J Appl Physiol. 2012;112:3787-95.
33. Kop WJ, Weissman NJ, Zhu J, Bonsall RW, Doyle M, Stretch MR, et al. Effects of acute mental stress and exercise on inflammatory markers in patients with coronary artery disease and healthy controls. Am J Cardiol. 2008;101:767-73.
34. Barnes JN, Trombold JR, Dhindsa M, Lin HF, Tanaka H. Arterial stiffening following eccentric exercise-induced muscle damage. J Appl Physiol. 2010;109:1102-8.
35. Vella LD, Caldow MK, Larsen AE, Tassoni D, Della Gatta PA, Gran P, et al. Resistance exercise increases nuclear factor-kappa B activity in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol. 2012;302:R667-73.
36. Ogawa K, Sanada K, Machida S, Okutsu M, Suzuki K. Resistance exercise training-induced muscle hypertrophy was associated with reduction of inflammatory markers in elderly women. Mediators Inflamm. 2010;2010:171023.
37. Mattusch F, Dufaux B, Heine O, Mertens I, Rost R. Reduction of the plasma concentration of C-reactive protein following nine months of endurance training. Int J Sports Med. 2000;21:21-4.
38. Myers JN, White JJ, Narasimhan B, Dalman RL. Effects of exercise training in patients with abdominal aortic aneurysm: preliminary results from a randomized trial. J Cardiopulm Rehabil Prev. 2010;30:374-83.
39. Milani RV, Lavie CJ, Mehra MR. Reduction in C-reactive protein through cardiac rehabilitation and exercise training. J Am Coll Cardiol. 2004;43:1056-61.
40. McDermott MM, Tiukinhoy S, Greenland P, Liu K, Pearce WH, Guralnik JM, et al. A pilot exercise intervention to improve lower extremity functioning in peripheral arterial disease unaccompanied by intermittent claudication. J Cardiopulm Rehabil. 2004;24:187-96.
41. Arsenault BJ, Cote M, Cartier A, Lemieux I, Després JP, Ross R, et al. Effect of exercise training on cardiometabolic risk markers among sedentary, but metabolically healthy overweight or obese postmenopausal women with elevated blood pressure. Atherosclerosis. 2009;207:530-3.
42. Drexel H, Saely CH, Langer P, Loruenser G, Marte T, Risch L, et al. Metabolic and anti-inflammatory benefits of eccentric endurance exercise - a pilot study. Eur J Clin Invest. 2008;38:218-26.
43. 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;42:304-13.
44. Rauramaa R, Halonen P, Vaisanen SB, Lakka TA, Schmidt-Trucksäss A, Berg A, et al. Effects of aerobic physical exercise on inflammation and atherosclerosis in men: the DNASCO Study: a six-year randomized, controlled trial. Ann Intern Med. 2004;140:1007-14.
45. Hammett CJ, Prapavessis H, Baldi JC, Varo N, Schoenbeck U, Ameratunga R, et al. Effects of exercise training on 5 inflammatory markers associated with cardiovascular risk. Am Heart J. 2006;151:367.
46. Lara Fernandes J, Serrano CV Jr, Toledo F, Hunziker MF, Zamperini A, Teo FH, et al. Acute and chronic effects of exercise on inflammatory markers and B-type natriuretic peptide in patients with coronary artery disease. Clin Res Cardiol. 2011;100:77-84.
47. Wilund KR, Tomayko EJ, Wu PT, Ryong Chung H, Vallurupalli S, Lakshminarayanan B, et al. Intradialytic exercise training reduces oxidative stress and epicardial fat: a pilot study. Nephrol Dial Transplant. 2010;25:2695-701.
48. Balen S, Vukelic-Damijani N, Persic V, Ruzić A, Miletić B, Samardiija M, et al. Anti-inflammatory effects of exercise training in the early period after myocardial infarction. Coll Antropol. 2008;32:285-91.
49. Gielen S, Adams V, Linke A, Erbs S, Möbius-Winkler S, Schubert A, et al. Exercise training in chronic heart failure: correlation between reduced local inflammation and improved oxidative capacity in the skeletal muscle. Eur J Cardiovasc Prev Rehabil. 2005;12:393-400.
50. Niebauer J, Clark AL, Webb-Peploe KM, Coats AJ. Exercise training in chronic heart failure: effects on pro-inflammatory markers. Eur J Heart Fail. 2005;7:189-93.
51. LeMaitre JP, Harris S, Fox KA, Denvir M. Change in circulating cytokines after 2 forms of exercise training in chronic stable heart failure. Am Heart J. 2004;147:100-5.
52. Gielen S, Adams V, Mobius-Winkler S, Linke A, Erbs S, Yu J, et al. Anti-inflammatory effects of exercise training in the skeletal muscle of patients with chronic heart failure. J Am Coll Cardiol. 2003;42:861-8.
53. Tisi PV, Hulse M, Chulakadabba A, Gosling P, Shearman CP. Exercise training for intermittent claudication: does it adversely affect biochemical markers of the exercise-induced inflammatory response? Eur J Vasc Endovasc Surg. 1997;14:344-50.
54. Lamina S, Okoye CG, Dagogo TT. Therapeutic effect of an interval exercise training program in the management of erectile dysfunction in hypertensive patients. J Clin Hypertens (Greenwich). 2009;11:125-9.
55. Pullen PR, Nagamia SH, Mehta PK, Thompson WR, Benardot D, Hammoud R, et al. Effects of yoga on inflammation and exercise capacity in patients with chronic heart failure. J Card Fail. 2008;14:407-13.
56. Pierce GL, Schofield RS, Casey DP, Hamlin SA, Hill JA, Braith RW. Effects of exercise training on forearm and calf vasodilation and proinfl ammatory markers in recent heart transplant recipients: a pilot study. Eur J Cardiovasc Prev Rehabil. 2008;15:10-18.
57. Meyer AA, Kundt G, Lenschow U, Schuff-Werner P, Kienast W. Improvement of early vascular changes and cardiovascular risk factors in obese children after a six-month exercise program. J Am Coll Cardiol. 2006;48:1865-70.
58. Nawaz S, Walker RD, Wilkinson CH, Saxton JM, Pockley AG, Wood RF. The inflammatory response to upper and lower limb exercise and the effects of exercise training in patients with claudication. J Vasc Surg. 2001;33:392-9.
59. Peschel T, Sixt S, Beitz F, Sonnabend M, Muth G, Thiele H, et al. High, but not moderate frequency and duration of exercise training induces downregulation of the expression of inflammatory and atherogenic adhesion molecules. Eur J Cardiovasc Prev Rehabil. 2007;14:476-82.
60. Giallauria F, Cirillo P, D'agostino M, Petrillo G, Vitelli A, Pacileo M, et al. Effects of exercise training on high-mobility group box-1 levels after acute myocardial infarction. J Card Fail. 2011;17:108-14.
61. Walther C, Mobius-Winkler S, Linke A, Bruegel M, Thiery J, Schuler G, 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;15:107-12.
62. Czepluch FS, Barres R, Caidahl K, Olieslagers S, Krook A, Rickenlund A, et al. Strenuous physical exercise adversely affects monocyte chemotaxis. Thromb Haemost. 2011;105:122-30.
63. Byrkjeland R, Nilsson BB, Westheim AS, Arnesen H, Seljeflot I. Inflammatory markers as related to disease severity in patients with chronic heart failure: limited effects of exercise training. Scand J Clin Lab Invest. 2011;71:598-605.
64. Pedersen BK, Febbraio MA. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev. 2008;88:1379-406.
65. Kestin AS, Ellis PA, Barnard MR, Errichetti A, Rosner BA, Michelson AD. Effect of strenuous exercise on platelet activation state and reactivity. Circulation. 1993;88:1502-11.
66. Wang JS. Exercise prescription and thrombogenesis. J Biomed Sci. 2006;13:753-61.
67. Wang JS, Jen CJ, Chen HI. Effects of exercise training and deconditioning on platelet function in men. Arterioscler Thromb Vasc Biol. 1995;15:1668-74.
68. Chen YW, Chen JK, Wang JS. Strenuous exercise promotes shear-induced thrombin generation by increasing the shedding of procoagulant microparticles from platelets. Thromb Haemost. 2010;104:293-301.
69. El-Sayed MS. Effects of exercise on blood coagulation, fibrinolysis and platelet aggregation. Sports Med. 1996;22:282-98.
70. Weiss C, Seitel G, Bartsch P. Coagulation and fibrinolysis after moderate and very heavy exercise in healthy male subjects. Med Sci Sports Exerc. 1998;30:246-51.
71. El-Sayed MS, Ali N, El-Sayed AZ. Aggregation and activation of blood platelets in exercise and training. Sports Med. 2005;35:11-22.
72. Wang JS, Jen CJ, Kung HC, Lin LJ, Hsiue TR, Chen HI. Different effects of strenuous exercise and moderate exercise on platelet function in men. Circulation. 1994;90:2877-85.
73. Wang JS, Cheng LJ. Effect of strenuous, acute exercise on alpha2-adrenergic agonist-potentiated platelet activation. Arterioscler Thromb Vasc Biol. 1999;19:1559-65.
74. Wang JS, Jen CJ, Lee HL, Chen HI. Effects of short-term exercise on female platelet function during different phases of the menstrual cycle. Arterioscler Thromb Vasc Biol. 1997;17:1682-6.
75. Albano AJ, Thompson PD, Kapur NK. Acute coronary thrombosis in Boston marathon runners. N Engl J Med. 2012;366:184-5.
76. Mazzeo RS. Catecholamine responses to acute and chronic exercise. Med Sci Sports Exerc. 1991;23:839-45.
77. Wang JS, Chow SE. Effects of exercise training and detraining on oxidized low-density lipoprotein-potentiated platelet function in men. Arch Phys Med Rehabil. 2004;85:1531-7.
78. Wang JS, Jen CJ, Chen HI. Effects of chronic exercise and deconditioning on platelet function in women. J Appl Physiol. 1997;83:2080-5.
79. El-Sayed MS, Lin X, Rattu AJ. Blood coagulation and fibrinolysis at rest and in response to maximal exercise before and after a physical conditioning programme. Blood Coagul Fibrinolysis. 1995;6:747-52.
80. El-Sayed MS. Effects of high and low intensity aerobic conditioning programs on blood fibrinolysis and lipid profile. Blood Coagul Fibrinolysis. 1996;7:484-90.
81. Sossdorf M, Otto GP, Claus RA, Gabriel HH, Losche W. Cell-derived microparticles promote coagulation after moderate exercise. Med Sci Sports Exerc. 2011;43:1169-76.
82. Pollock ML, Franklin BA, Balady GJ, Chaitman BL, Fleg JL, Fletcher B, et al. AHA Science Advisory. Resistance exercise in individuals with and without cardiovascular disease: benefits, rationale, safety, and prescription: An advisory from the Committee on Exercise, Rehabilitation, and Prevention, Council on Clinical Cardiology, American Heart Association; Position paper endorsed by the American College of Sports Medicine. Circulation. 2000;101:828-33.
83. de Jong AT, Womack CJ, Perrine JA, Franklin BA. Hemostatic responses to resistance training in patients with coronary artery disease. J Cardiopulmon Rehabil. 2006;26:80-3.
84. El-Sayed MS. Fibrinolytic and hemostatic response after resistance exercise. Med Sci Sports Exerc. 1993;25:597-602.
85. Petidis K, Douma S, Doumas M, Basagiannis I, Vogiatzis K, Zamboulis C. The interaction of vasoactive substances during exercise modulates platelet aggregation in hypertension and coronary artery disease. BMC Cardiovasc Disord. 2008;8:11.
86. Ahmadizad S, El-Sayed MS. The effects of graded resistance exercise on platelet aggregation and activation. Med Sci Sports Exerc. 2003;35:1026-32.
87. Kratz A, Wood MJ, Siegel AJ, Hiers JR, Van Cott EM. Effects of marathon running on platelet activation markers: direct evidence for in vivo platelet activation. Am J Clin Pathol. 2006;125:296-300.
88. Plaisance EP, Taylor JK, Alhassan S, Abebe A, Mestek ML, Grandjean PW. Cardiovascular fitness and vascular inflammatory markers after acute aerobic exercise. Int J Sport Nutr Exerc Metab. 2007;17:152-62.
89. Kobusiak-Prokopowicz M, Kuliczkowski W, Karolko B, Prajs I, Mazurek W. Platelet aggregation and P-selectin levels during exercise treadmill test in patients with ischaemic heart disease. Kardiol Pol. 2006;64:1094-100.
90. Placanica G, Migliau G, Nasso G, Rosso R, Tallarico D, Migliau G. Short-term effect of exercise on platelet factor 4 in normal subjects and in patients with coronary artery disease. Cardiologia. 1999;44:993-6.
91. Wang JS. Intense exercise increases shear-induced platelet aggregation in men through enhancement of von Willbrand factor binding, glycoprotein IIb/IIIa activation, and P-selectin expression on platelets. Eur J Appl Physiol. 2004;91:741-7.
92. Menzel K, Hilberg T. Blood coagulation and fibrinolysis in healthy, untrained subjects: effects of different exercise intensities controlled by individual anaerobic threshold. Eur J Appl Physiol. 2011;111:253-60.
93. Burns P, Wilmink T, Fegan C, Bradbury AW. Exercise in claudicants is accompanied by excessive thrombin generation. Eur J Vasc Endovasc Surg. 2003;26:150-5.
94. Menzel K, Hilberg T. Coagulation and fibrinolysis are in balance after moderate exercise in middle-aged participants. Clin Appl Thromb Hemost. 2009;15:348-55.
95. Hilberg T, Glaser D, Reckhart C, Prasa D, Sturzebecher J, Gabriel HH. Blood coagulation and fibrinolysis after long-duration treadmill exercise controlled by individual anaerobic threshold. Eur J Appl Physiol. 2003;90:639-42.
96. Hilberg T, Prasa D, Sturzebecher J, Glaser D, Scheider K, Gabriel HH. Blood coagulation and fibrinolysis after extreme short-term exercise. Thromb Res. 2003;109:271-7.
97. Womack CJ, Rasmussen JM, Vickers DG, Paton CM, Osmond PJ, Davis GL. Changes in fibrinolysis following exercise above and below lactate threshold. Thromb Res. 2006;118:263-8.
98. Ivey FM, Womack CJ, Kulaputana O, Dobrovolny CL, Wiley LA, Macko RF. A single bout of walking exercise enhances endogenous fibrinolysis in stroke patients. Med Sci Sports Exerc. 2003;35:193-8.
99. Andreotti F, Lanza GA, Sciahbasi A, Fischetti D, Sestito A, De Cristofaro R, et al. Low-grade exercise enhances platelet aggregability in patients with obstructive coronary disease independently of myocardial ischemia. Am J Cardiol. 2001;87:16-20.
100. Thrall G, Lip GY. Exercise and the prothrombotic state: a paradox of cardiovascular prevention or an enhanced prothrombotic state? Arterioscler Thromb Vasc Biol. 2005;25:265-6.
101. Freedman JE. Resistance training: does it alter lytic potential? J Cardiopulm Rehabil. 2006;26:84-5.
102. Nagelkirk PR, Scalzo R, Harber M, Kaminsky LA. The influence of acute resistance training and body composition on coagulation and fibrinolytic activity in low-risk women. Int J Sports Med. 2010;31:458-62.
103. Kokkinos P, Myers J. Exercise and physical activity: clinical outcomes and applications. Circulation. 2010;122:1637-48.
104. Wang JS, Li YS, Chen JC, Chen YW. Effects of exercise training and deconditioning on platelet aggregation induced by alternating shear stress in men. Arterioscler Thromb Vasc Biol. 2005;25:454-60.
105. Di Massimo C, Scarpelli P, Penco M, Tozzi-Ciancarelli MG. Possible involvement of plasma antioxidant defences in training-associated decrease of platelet responsiveness in humans. Eur J Appl Physiol. 2004;91:406-12.
106. Ferguson EW, Bernier LL, Banta GR, Yu-Yahiro J, Schoomaker EB. Effects of exercise and conditioning on clotting and fibrinolytic activity in men. J Appl Physiol. 1987;62:1416-21.
107. Ponjee GA, Janssen GM, van Wersch JW. Prolonged endurance exercise and blood coagulation: a 9 month prospective study. Blood Coagul Fibrinolysis. 1993;4:21-5.
108. Jahangard T, Torkaman G, Ghoosheh B, Hedayati M, Dibaj A. The effect of short-term aerobic training on coagulation and fibrinolytic factors in sedentary healthy postmenopausal women. Maturitas. 2009;64:223-7.
109. Clark BC, Manini TM, Hoffman RL, Williams PS, Guiler MK, Knutson MJ, et al. Relative safety of 4 weeks of blood flow-restricted resistance exercise in young, healthy adults. Scand J Med Sci Sports. 2011;21:653-62.
110. Bye A, Tjonna AE, Stolen TO, Rosbjorgen RE, Wisloff U. Transcriptional changes in blood after aerobic interval training in patients with the metabolic syndrome. Eur J Cardiovasc Prev Rehabil. 2009;16:47-52.
111. Lominadze D, Dean WL, Tyagi SC, Roberts AM. Mechanisms of fibrinogen-induced microvascular dysfunction during cardiovascular disease. Acta Physiol (Oxf). 2010;198:1-13.
112. Lira FS, Carnevali LC, Zanchi NE, Santos RVT, Lavoie JM, Seelaender M. Exercise intensity modulation of hepatic lipid metabolism. J Nutr Metab. 2012;2012:809576.
113. Petersen AM, Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol. 2005;98:1154-62.
114. Chaar V, Romana M, Tripette J, Broquere C, Huisse MG, Hue O, et al. Effect of strenuous physical exercise on circulating cell-derived microparticles. Clin Hemorheol Microcirc. 2011;47:15-25.
115. Mesri M, Altieri DC. Endothelial cell activation by leukocyte microparticles. J Immunol. 1998;161:4382-7.
116. Geertsema L, Lucas SJ, Cotter JD, Hock B, McKenzie J, Fernyhough LJ. The cardiovascular risk factor, soluble CD40 ligand (CD154), but not soluble CD40 is lowered by ultra-endurance exercise in athletes. Br J Sports Med. 2011;45:42-5.
117. Bjornstad HH, Bruvik J, Bjornstad AB, Hjellestad BL, Damas JK, Aukrust P. Exercise training decreases plasma levels of soluble CD40 ligand and P-selectin in patients with chronic heart failure. Eur J Cardiovasc Prev Rehabil. 2008;15:43-8.
118. Simpson KA, Singh MAF. Effects of exercise on adiponectin: a systematic review. Obesity. 2008;16:241-56.
119. Eriksson M, Johnson O, Boman K, Hallmans G, Hellsten G, Nilsson TK, et al. Improved fibrinolytic activity during exercise may be an effect of the adipocyte-derived hormones leptin and adiponectin. Thromb Res. 2008;122:701-8.
120. Mansouri M, Keshtkar A, Hasani-Ranjbar S, Soleymani Far E, Tabatabaei-Malazy O, Omidfar K, et al. The impact of one session resistance exercise on plasma adiponectin and RBP4 concentration in trained and untrained healthy young men. Endocr J. 2011;58:861-8.
121. Wang JS, Yen HL, Yang CM. Warm-up exercise suppresses platelete-osinophil/neutrophil aggregation and platelet-promoted release of eosinophil/neutrophil oxidant products enhanced by severe exercise in men. Thromb Haemost. 2006;95:490-8.
122. Milias GA, Nomikos T, Fragopoulou E, Athanasopoulos S, Antonopoulou S. Effects of eccentric exercise-induced muscle injury on blood levels of platelet activating factor (PAF) and other inflammatory markers. Eur J Appl Physiol. 2005;95:504-13.
123. Connolly PH, Caiozzo VJ, Zaldivar F, Nemet D, Larson J, Hung SP, et al. Effects of exercise on gene expression in human peripheral blood mononuclear cells. J Appl Physiol. 2004;97:1461-9.
124. Gulmez O, Ertan C, Yildirir A, Konas D, Bal U, Aydinalp A, et al. C-reactive protein levels increase after exercise testing in patients with increased platelet reactivity. Coron Artery Dis. 2007;18:437-42.
125. de Meirelles LR, Mendes-Ribeiro AC, Mendes MA, da Silva MN, Ellory JC, Mann GE, et al. Chronic exercise reduces platelet activation in hypertension: upregulation of the L-arginine-nitric oxide pathway. Scand J Med Sci Sports. 2009;19:67-74.
126. Cuzzolin L, Lussignoli S, Crivellente F, Adami A, Schena F, Bellavite P, et al. Influence of an acute exercise on neutrophil and platelet adhesion, nitric oxide plasma metabolites in inactive and active subjects. Int J Sports Med. 2000;21:289-93.
127. Foster NK, Martyn JB, Rangno RE, Hogg JC, Pardy RL. Leukocytosis of exercise: role of cardiac output and catecholamines. J Appl Physiol. 1986;61:2218-23.
128. Li N, Wallen H, Hjemdahl P. Evidence for prothrombotic effects of exercise and limited protection by aspirin. Circulation. 1999;100:1374-9.
129. Robert L. Aging of the vascular wall and atherogenesis: role of the elastin-laminin receptor. Atherosclerosis. 1996;123:169-79.
130. Guarnieri C, Melandri G, Caldarera I, Cervi V, Semprini F, Branzi A. Spontaneous superoxide generation by polymorphonuclear leukocytes isolated from patients with stable angina after physical exercise. Int J Cardiol. 1992;37:301-7.
131. Rainer C, Kawanishi DT, Chandraratna PA, Bauersachs RM, Reid CL, Rahimtoola SH, et al. Changes in blood rheology in patients with stable angina pectoris as a result of coronary artery disease. Circulation. 1987;76:15-20.
132. Berliner S, Rogowski O, Aharonov S, Mardi T, Tolshinsky T, Rozenblat M, et al. Erythrocyte adhesiveness/aggregation: a novel biomarker for the detection of low-grade internal inflammation in individuals with atherothrombotic risk factors and proven vascular disease. Am Heart J. 2005;149:260-7.
133. Baskurt OK, Temiz A, Meiselman HJ. Effect of superoxide anions on red blood cell rheologic properties. Free Radic Biol Med. 1998;24:102-10.
134. Brun JF, Khaled S, Raynaud E, Bouix D, Micallef JP, Orsetti A. The triphasic effects of exercise on blood rheology: which relevance to physiology and pathophysiology? Clin Hemorheol. 1998;19:89-104.
135. Gueguen-Duchesne M, Durand F, Beillot J, Dezier JF, Rochcongar P, Le Goff MC, et al. Could maximal exercise be a hemorheological risk factor? Clin Hemorheol. 1987;7:418.
136. Brun JF, Micallef JP, Orsetti A. Hemorheologic effects of light prolonged exercise. Clin Hemorheol. 1994;14:807-18.
137. Nageswari K, Banerjee R, Gupte RV, Puniyani RR. Effects of exercise on rheological and microcirculatory parameters. Clin Hemorheol Microcirc. 2000;23:243-7.
138. Yalcin O, Erman A, Muratli S, Bor-Kucukatay M, Baskurt K. Time course of hemorheological alterations after heavy anaerobic exercise in untrained human subjects. J Appl Physiol. 2003;94:997-1002.
139. Tripette J, Connes P, Beltan E, Chalabi T, Marlin L, Chout R, et al. Red blood cell deformability and aggregation, cell adhesion molecules, oxidative stress and nitric oxide markers after a short term, submaximal, exercise in sickle cell trait carriers. Clin Hemorheol Microcirc. 2010;45:39-52.
140. Suhr F, Porten S, Hertrich T, Brixius K, Schmidt A, Platen P, et al. Intensive exercise induces changes of endothelial nitric oxide synthase pattern in human erythrocytes. Nitric Oxide. 2009;20:95-103.
141. Baskurt OK, Ulker P, Meiselman HJ. Nitric oxide, erythrocytes and exercise. Clin Hemorheol Microcirc. 2011;49:175-81.
142. Neuhaus D, Gaehtgens P. Haemorheology and long term exercise. Sports Med. 1994;18:10-21.
143. El-Sayed MS. Effects of exercise and training on blood rheology. Sports Med. 1998;26:281-92.
144. Smith JA. Exercise, training and red blood cell turnover. Sports Med. 1995;19:9-31.
145. Bouchard C, Blair SN, Church TS, Earnest CP, Hagberg JM, Häkkinen K, et al. Adverse metabolic response to regular exercise: is it a rare or common occurrence? PLoS One. 2012;7:e37887.