Vascular effects of exercise training in CKD: Current evidence and pathophysiological mechanisms

Clinical Journal of the American Society of Nephrology

Volumn 9, Issue 7, 2014, Pages 1305-1318

  Van Craenenbroeck, Amaryllis H ^a,b   Van Craenenbroeck, Emeline M ^a,b   Kouidi, Evangelia ^c   Vrints, Christiaan J ^a,b   Couttenye, Marie M ^a   Conraads, Viviane M ^a,b  

^a ANTWERP UNIVERSITY HOSPITAL   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; C REACTIVE PROTEIN; CATALASE; CAVEOLIN 1; DIMETHYLARGININASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUTATHIONE PEROXIDASE; GLUTHATIONE; HEAT SHOCK PROTEIN 90; INTERLEUKIN 6; N (G), N (G) DIMETHYLARGININE; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ARTERIAL STIFFNESS; ATHEROSCLEROSIS; BLOOD PRESSURE; CHRONIC KIDNEY DISEASE; END STAGE RENAL DISEASE; ENDOTHELIAL DYSFUNCTION; ENDOTHELIAL PROGENITOR CELL; ENZYME ACTIVITY; EXERCISE; HUMAN; MORTALITY; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RISK FACTOR; TISSUE REPAIR; VASCULAR DISEASE; ANIMAL; ARTERY; COMORBIDITY; HEMODYNAMICS; KINESIOTHERAPY; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; RENAL INSUFFICIENCY, CHRONIC; TREATMENT OUTCOME; VASCULAR DISEASES;

ANIMALS; ARTERIES; COMORBIDITY; EXERCISE THERAPY; HEMODYNAMICS; HUMANS; RENAL INSUFFICIENCY, CHRONIC; RISK FACTORS; TREATMENT OUTCOME; VASCULAR DISEASES;

EID: 84923768115     PISSN: 15559041     EISSN: 1555905X     Source Type: Journal    
DOI: 10.2215/CJN.13031213     Document Type: Review

References (70)

1. Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY: Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med 351: 1296–1305, 2004
2. Culleton BF, Larson MG, Wilson PW, Evans JC, Parfrey PS, Levy D: Cardiovascular disease andmortality in a communitybased cohort with mild renal insufficiency. Kidney Int 56: 2214–2219, 1999
3. Foley RN, Parfrey PS, Sarnak MJ : Epidemiology of cardiovascular disease in chronic renal disease. J Am Soc Nephrol 9[Suppl]: S16–S23, 1998
4. Matsushita K, vander Velde M, Astor BC, Woodward M, Levey AS, de Jong PE, Coresh J, Gansevoort RT; Chronic Kidney Disease Prognosis Consortium: Association of estimated glomerular filtration rate and albuminuria with all-cause and cardiovascular mortality in general population cohorts: A collaborative metaanalysis. Lancet 375: 2073–2081, 2010
5. Sarnak MJ: Cardiovascular complications in chronic kidney disease. Am J Kidney Dis 41[Suppl]: 11–17, 2003
6. Perk J, De Backer G, Gohlke H, Graham I, Reiner Z, Verschuren M, Albus C, Benlian P, Boysen G, Cifkova R, Deaton C, Ebrahim S, Fisher M, Germano G, Hobbs R, Hoes A, Karadeniz S, Mezzani A, Prescott E, Ryden L, Scherer M, Syvänne M, Scholte op Reimer WJ, Vrints C, Wood D, Zamorano JL, Zannad F; European Association for Cardiovascular Prevention & Rehabilitation (EACPR); ESC Committee for Practice Guidelines (CPG): European Guidelines on cardiovascular disease prevention in clinical practice (version 2012). The Fifth Joint Task Force of the European Society of Cardiology andOther Societies on Cardiovascular Disease Prevention in Clinical Practice (constituted by representatives of nine societies and by invited experts). Eur Heart J 33: 1635–1701, 2012
7. National Kidney Foundation: K/DOQI clinical practice guidelines for chronic kidney disease: Evaluation, classification, and stratification. Am J Kidney Dis 39[Suppl 1]: S1–S266, 2002
8. Stenvinkel P, Carrero JJ, Axelsson J, Lindholm B, Heimburger O, Massy Z: Emerging biomarkers for evaluating cardiovascular risk in the chronic kidney disease patient: How do new pieces fit into the uremic puzzle? Clin J AmSoc Nephrol 3: 505–521, 2008
9. Gielen S, Schuler G, Adams V: Cardiovascular effects of exercise training: Molecular mechanisms. Circulation 122: 1221–1238, 2010
10. Eckel RH, Jakicic JM, Ard JD, Hubbard VS, de Jesus JM, Lee IM, Lichtenstein AH, Loria CM, Millen BE, Miller NH, Nonas CA, Sacks FM, Smith SC Jr., Svetkey LP, Wadden TW, Yanovski SZ: 2013 AHA/ACC guideline on lifestyle management to reduce cardiovascular risk: A report of the American College of Cardiology American Heart Association Task Force on Practice Guidelines [published online ahead of print November 12, 2013]. Circulation
11. Gansevoort RT, Correa-Rotter R, Hemmelgarn BR, Jafar TH, Heerspink HJ, Mann JF, Matsushita K, Wen CP: Chronic kidney disease and cardiovascular risk: Epidemiology, mechanisms, and prevention. Lancet 382: 339–352, 2013
12. Briet M, Burns KD: Chronic kidney disease and vascular remodelling: Molecular mechanisms and clinical implications. Clin Sci (Lond) 123: 399–416, 2012
13. Ross R: Atherosclerosis—an inflammatory disease. N Engl J Med 340: 115–126, 1999
14. Stam F, van Guldener C, Becker A, Dekker JM, Heine RJ, Bouter LM, Stehouwer CD: Endothelial dysfunction contributes to renal function-associated cardiovascular mortality in a population with mild renal insufficiency: The Hoorn study. J AmSoc Nephrol 17: 537–545, 2006
15. London GM, Blacher J, Pannier B, Guerin AP, Marchais SJ, Safar ME: Arterial wave reflections and survival in end-stage renal failure. Hypertension 38: 434–438, 2001
16. Garcia-Cardena G, Gimbrone MA Jr.: Biomechanical modulation of endothelial phenotype: Implications for health and disease. Handb Exp Pharmacol 176 Pt2: 79–95, 2006
17. Schuler G, Adams V, Goto Y: Role of exercise in the prevention of cardiovascular disease: Results, mechanisms, and new perspectives. Eur Heart J 34: 1790–1799, 2013
18. Roshanravan B, Robinson-Cohen C, Patel KV, Ayers E, Littman AJ, de Boer IH, Ikizler TA, Himmelfarb J, Katzel LI, Kestenbaum B, Seliger S: Association between physical performance and allcause mortality in CKD. J Am Soc Nephrol 24: 822–830, 2013
19. Wang IK, Tsai MK, Liang CC, Yen TH, Huang CC, Wen SF, Wen CP: The role of physical activity in chronic kidney disease in the presence of diabetes mellitus: A prospective cohort study. Am J Nephrol 38: 509–516, 2013
20. Johansen KL, Kaysen GA,Dalrymple LS, Grimes BA, GliddenDV, Anand S, Chertow GM: Association of physical activity with survival among ambulatory patients on dialysis: The Comprehensive Dialysis Study. Clin J Am Soc Nephrol 8: 248–253, 2013
21. Sietsema KE, Amato A, Adler SG, Brass EP: Exercise capacity as a predictor of survival among ambulatory patients with end-stage renal disease. Kidney Int 65: 719-724, 2004
22. Lee DC, Sui X, Ortega FB, Kim YS, Church TS, Winett RA, Ekelund U, Katzmarzyk PT, Blair SN: Comparisons of leisuretime physical activity and cardiorespiratory fitness as predictors of all-cause mortality in men and women. Br J Sports Med 45: 504–510, 2011
23. Myers J, Kaykha A, George S, Abella J, Zaheer N, Lear S, Yamazaki T, Froelicher V: Fitness versus physical activity patterns in predicting mortality in men. Am J Med 117: 912–918, 2004
24. Johansen KL, Painter P: Exercise in individuals with CKD. Am J Kidney Dis 59: 126–134, 2012
25. Blacher J, Asmar R, Djane S, London GM, Safar ME: Aortic pulse wave velocity as a marker of cardiovascular risk in hypertensive patients. Hypertension 33: 1111–1117, 1999
26. Guerin AP, Blacher J, Pannier B, Marchais SJ, Safar ME, London GM: Impact of aortic stiffness attenuation on survival of patients in end-stage renal failure. Circulation 103: 987–992, 2001
27. Mustata S, ChanC, Lai V, Miller JA: Impact of an exercise program on arterial stiffness and insulin resistance in hemodialysis patients. J Am Soc Nephrol 15: 2713-2718, 2004
28. Toussaint ND, Polkinghorne KR, Kerr PG: Impact of intradialytic exercise on arterial compliance and B-type natriuretic peptide levels in hemodialysis patients. Hemodial Int 12: 254–263, 2008
29. Koh KP, Fassett RG, Sharman JE, Coombes JS, Williams AD: Effect of intradialytic versus home-based aerobic exercise training on physical function and vascular parameters in hemodialysis patients: A randomized pilot study. Am J Kidney Dis 55: 88-99, 2010
30. Mustata S, Groeneveld S, Davidson W, Ford G, Kiland K, Manns B: Effects of exercise training on physical impairment, arterial stiffness and health-related quality of life in patients with chronic kidney disease: A pilot study. Int Urol Nephrol 43: 1133-1141, 2011
31. Hambrecht R, Wolf A, Gielen S, Linke A, Hofer J, Erbs S, Schoene N, Schuler G: Effect of exercise on coronary endothelial function in patients with coronary artery disease. N Engl J Med 342: 454–460, 2000
32. Shelkovnikov S, Summers SM, Elahimehr R, Adams G, Purdy RE, Vaziri ND: Effect of exercise training on aortic tone in chronic renal insufficiency. Am J Hypertens 21: 564–569, 2008
33. Cornelissen VA, Smart NA: Exercise training for blood pressure: A systematic review and meta-analysis. J Am Heart Assoc 2: e004473, 2013
34. Heiwe S, Jacobson SH: Exercise training for adults with chronic kidney disease. Cochrane Database Syst Rev 10: CD003236, 2011
35. Vane JR, Anggard EE, Botting RM: Regulatory functions of the vascular endothelium. N Engl J Med 323: 27–36, 1990
36. Goligorsky MS, Li H, Brodsky S, Chen J: Relationships between caveolae and eNOS: Everything in proximity and the proximity of everything. Am J Physiol Renal Physiol 283: F1–F10, 2002
37. Balligand JL, Feron O, Dessy C : eNOS activation by physical forces: From short-term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol Rev 89: 481–534, 2009
38. Sindhu RK, Ehdaie A, Vaziri ND, Roberts CK: Effects of chronic renal failure on caveolin-1, guanylate cyclase and AKT protein expression. Biochim Biophys Acta 1690: 231–237, 2004
39. Zoccali C, Bode-Böger S, Mallamaci F, Benedetto F, Tripepi G, Malatino L, Cataliotti A, Bellanuova I, Fermo I, Frölich J, Böger R: Plasma concentration of asymmetrical dimethylarginine and mortality in patients with end-stage renal disease: A prospective study. Lancet 358: 2113–2117, 2001
40. Fliser D, Kronenberg F, Kielstein JT, Morath C, Bode-Böger SM, Haller H, Ritz E: Asymmetric dimethylarginine and progression of chronic kidney disease: The mild to moderate kidney disease study. J Am Soc Nephrol 16: 2456–2461, 2005
41. Schwedhelm E, Böger RH: The role of asymmetric and symmetric dimethylarginines in renal disease. Nat Rev Nephrol 7: 275–285, 2011
42. Hambrecht R, Adams V, Erbs S, Linke A, Kränkel N, Shu Y, Baither Y, Gielen S, Thiele H, Gummert JF, Mohr FW, Schuler G: Regular physical activity improves endothelial function in patients with coronary artery disease by increasing phosphorylation of endothelial nitric oxide synthase. Circulation 107: 3152–3158, 2003
43. Sindler AL, Delp MD, Reyes R, Wu G, Muller-Delp JM: Effects of ageing and exercise training on eNOS uncoupling in skeletal muscle resistance arterioles. J Physiol 587: 3885–3897, 2009
44. Richter B, Niessner A, Penka M, Grdic M, Steiner S, Strasser B, Ziegler S, Zorn G, Maurer G, SimeonRudolf V, Wojta J, Huber K: Endurance training reduces circulating asymmetric dimethylarginine and myeloperoxidase levels in persons at risk of coronary events. Thromb Haemost 94: 1306–1311, 2005
45. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM: Isolation of putative progenitor endothelial cells for angiogenesis. Science 275: 964–967, 1997
46. Lorenzen J, David S, Bahlmann FH, de Groot K, Bahlmann E, Kielstein JT, Haller H, Fliser D: Endothelial progenitor cells and cardiovascular events in patients with chronic kidney disease—a prospective follow-up study. PLoS ONE 5: e11477, 2010
47. Van Craenenbroeck EM, Van Craenenbroeck AH, van Ierssel S, Bruyndonckx L, Hoymans VY, Vrints CJ, Conraads VM: Quantification of circulating CD34+/KDR+/CD45dim endothelial progenitor cells: Analytical considerations. Int J Cardiol 167: 1688–1695, 2013
48. Mayr M, Niederseer D, Niebauer J: Frombench to bedside: What physicians need to know about endothelial progenitor cells. AmJ Med 124: 489–497, 2011
49. Volaklis KA, Tokmakidis SP, Halle M: Acute and chronic effects of exercise on circulating endothelial progenitor cells in healthy and diseased patients. Clin Res Cardiol 102: 249–257, 2013
50. Manfredini F, Rigolin GM, Malagoni AM, Catizone L, Mandini S, Sofritti O, Mauro E, Soffritti S, Boari B, Cuneo A, Zamboni P, Manfredini R: Exercise training and endothelial progenitor cells in haemodialysis patients. J IntMed Res 37: 534–540, 2009
51. Manfredini F, Rigolin GM, Malagoni AM, Soffritti S, Boari B, Conconi F, Castoldi GL, Catizone L, Zamboni P, Manfredini R: Exercise capacity and circulating endothelial progenitor cells in hemodialysis patients. Int J Sports Med 28: 368–373, 2007
52. Himmelfarb J, Stenvinkel P, Ikizler TA, Hakim RM: The elephant in uremia: Oxidant stress as a unifying concept of cardiovascular disease in uremia. Kidney Int 62: 1524-1538, 2002
53. Jourde-Chiche N, Dou L, Cerini C, Dignat-George F, Brunet P: Vascular incompetence in dialysis patients—protein-bound uremic toxins and endothelial dysfunction. Semin Dial 24: 327–337, 2011
54. de Souza PS, da Rocha LG, Tromm CB, Scheffer DL, Victor EG, da Silveira PC, de Souza CT, Silva LA, Pinho RA: Therapeutic action of physical exercise on markers of oxidative stress induced by chronic kidney disease. Life Sci 91: 132–136, 2012
55. Pechter U, Ots M, Mesikepp S, Zilmer K, Kullissaar T, Vihalemm T, Zilmer M, Maaroos J: Beneficial effects of water-based exercise in patients with chronic kidney disease. Int J Rehabil Res 26: 153–156, 2003
56. Wilund KR, Tomayko EJ, Wu PT, Ryong Chung H, Vallurupalli S, Lakshminarayanan B, Fernhall B: Intradialytic exercise training reduces oxidative stress and epicardial fat: A pilot study. Nephrol Dial Transplant 25: 2695–2701, 2010
57. Zoccali C, Tripepi G, Mallamaci F: Dissecting inflammation in ESRD: Do cytokines and C-reactive protein have a complementary prognostic value for mortality in dialysis patients? J Am Soc Nephrol 17[Suppl 3]: S169–S173, 2006
58. Heine GH, Ortiz A, Massy ZA, Lindholm B, Wiecek A, Martınez- Castelao A, Covic A, Goldsmith D, Suleymanlar G, London GM, Parati G, Sicari R, Zoccali C, Fliser D; European Renal and Cardiovascular Medicine (EURECA‑m) working group of the European Renal Association-European Dialysis and Transplant Association (ERA EDTA): Monocyte subpopulations and cardiovascular risk in chronic kidney disease. Nat Rev Nephrol 8: 362–369, 2012
59. Bostrom KI, Rajamannan NM, Towler DA: The regulation of valvular and vascular sclerosis by osteogenic morphogens. Circ Res 109: 564–577, 2011
60. Gleeson M, Bishop NC, Stensel DJ, Lindley MR, Mastana SS, Nimmo MA: The anti inflammatory effects of exercise: Mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol 11: 607–615, 2011
61. Castaneda C, Gordon PL, Parker RC, Uhlin KL, Roubenoff R, Levey AS: Resistance training to reduce the malnutritioninflammation complex syndrome of chronic kidney disease. Am J Kidney Dis 43: 607–616, 2004
62. Headley S, Germain M, Milch C, Pescatello L, Coughlin MA, Nindl BC, Cornelius A, Sullivan S, Gregory S, Wood R: Exercise training improves HR responses and V_O2peak in predialysis kidney patients. Med Sci Sports Exerc 44: 2392–2399, 2012
63. Leehey DJ, Moinuddin I, Bast JP, Qureshi S, Jelinek CS, Cooper C, Edwards LC, Smith BM, Collins EG: Aerobic exercise in obese diabetic patients with chronic kidney disease: A randomized and controlled pilot study. Cardiovasc Diabetol 8: 62, 2009
64. Afshar R, Emany A, Saremi A, Shavandi N, Sanavi S: Effects of intradialytic aerobic training on sleep quality in hemodialysis patients. Iran J Kidney Dis 5: 119–123, 2011
65. Kopple JD, Wang H, Casaburi R, Fournier M, Lewis MI, Taylor W, Storer TW: Exercise in maintenance hemodialysis patients induces transcriptional changes in genes favoring anabolic muscle. J Am Soc Nephrol 18: 2975–2986, 2007
66. Cheema B, Abas H, Smith B, O’Sullivan A, Chan M, Patwardhan A, Kelly J, Gillin A, Pang G, Lloyd B, Singh MF: Progressive exercise for anabolism in kidney disease (PEAK): A randomized, controlled trial of resistance training during hemodialysis. J Am Soc Nephrol 18: 1594–1601, 2007
67. Timmerman KL, Flynn MG, Coen PM, Markofski MM, Pence BD: Exercise training-induced lowering of inflammatory (CD14+CD16+) monocytes: A role in the anti inflammatory influence of exercise? J Leukoc Biol 84: 1271–1278, 2008
68. McFarlin BK, Flynn MG, Campbell WW, Stewart LK, Timmerman KL: TLR4 is lower in resistance-trained older women and related to inflammatory cytokines. Med Sci Sports Exerc 36: 1876–1883, 2004
69. K/DOQI Workgroup: K/DOQI clinical practice guidelines for cardiovascular disease in dialysis patients. Am J Kidney Dis 45 [Suppl 3]: S1–S153, 2005
70. Johansen KL: Exercise and dialysis. Hemodial Int 12: 290–300, 2008