Skip to main content

Effects of Catheterization on Artery Function and Health: When Should Patients Start Exercising Following Their Coronary Intervention?

Sports Medicine volume 49, pages 397–416 (2019)Cite this article

Abstract

Coronary artery disease (CAD) is a leading cause of death worldwide, and percutaneous transluminal coronary angiography (PTCA) and/or percutaneous coronary intervention (PCI; angioplasty) are commonly used to diagnose and/or treat the obstructed coronaries. Exercise-based rehabilitation is recommended for all CAD patients; however, most guidelines do not specify when exercise training should commence following PTCA and/or PCI. Catheterization can result in arterial dysfunction and acute injury, and given the fact that exercise, particularly at higher intensities, is associated with elevated inflammatory and oxidative stress, endothelial dysfunction and a pro-thrombotic milieu, performing exercise post-PTCA/PCI may transiently elevate the risk of cardiac events. This review aims to summarize extant literature relating to the impacts of coronary interventions on arterial function, including the time-course of recovery and the potential deleterious and/or beneficial impacts of acute versus long-term exercise. The current literature suggests that arterial dysfunction induced by catheterization recovers 4–12 weeks following catheterization. This review proposes that a period of relative arterial vulnerability may exist and exercise during this period may contribute to elevated event susceptibility. We therefore suggest that CAD patients start an exercise training programme between 2 and 4 weeks post-PCI, recognizing that the literature suggest there is a ‘grey area’ for functional recovery between 2 and 12 weeks post-catheterization. The timing of exercise onset should take into consideration the individual characteristics of patients (age, severity of disease, comorbidities) and the intensity, frequency and duration of the exercise prescription.

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

Access options

Buy single article

Instant access to the full article PDF.

USD 49.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2

References

  1. World Health Organisation, World Heart Federation, World Stroke Organization. Death and disability due to CVDs (heart attacks and strokes). Global Atlas on cardiovascular disease prevention and control. Policies, strategies and interventions. World Health Organisation; 2011. https://www.who.int/cardiovascular_diseases/publications/atlas_cvd/en/. Accessed 9 Sept 2017.

  2. Wu MY, Li CJ, Hou MF, Chu PY. New insights into the role of inflammation in the pathogenesis of atherosclerosis. Int J Mol Sci. 2017. https://doi.org/10.3390/ijms18102034.

    PubMed  PubMed Central  Article  Google Scholar 

  3. Falk E. Pathogenesis of atherosclerosis. J Am Coll Cardiol. 2006;47(8 Suppl):C7–12. https://doi.org/10.1016/j.jacc.2005.09.068.

    PubMed  CAS  Article  Google Scholar 

  4. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362(6423):801–9. https://doi.org/10.1038/362801a0.

    PubMed  CAS  Article  Google Scholar 

  5. Herrington W, Lacey B, Sherliker P, Armitage J, Lewington S. Epidemiology of atherosclerosis and the potential to reduce the global burden of atherothrombotic disease. Circ Res. 2016;118(4):535–46. https://doi.org/10.1161/circresaha.115.307611.

    PubMed  CAS  Article  Google Scholar 

  6. Mozaffarian D, Benjamin EJ, Go AS, Arnett DK, Blaha MJ, Cushman M, et al. Executive summary: heart disease and stroke statistics–2016 update: a report from the American Heart Association. Circulation. 2016;133(4):447–54. https://doi.org/10.1161/cir.0000000000000366.

    PubMed  Article  Google Scholar 

  7. Campeau L. Percutaneous radial artery approach for coronary angiography. Cathet Cardiovasc Diagn. 1989;16(1):3–7.

    PubMed  CAS  Article  Google Scholar 

  8. Montalescot G, Sechtem U, Achenbach S, Andreotti F, Arden C, Budaj A, et al. 2013 ESC guidelines on the management of stable coronary artery disease: the Task Force on the management of stable coronary artery disease of the European Society of Cardiology. Eur Heart J. 2013;34(38):2949–3003. https://doi.org/10.1093/eurheartj/eht296.

    PubMed  Article  Google Scholar 

  9. Kunadian V, Qiu W, Lagerqvist B, Johnston N, Sinclair H, Tan Y, et al. Gender differences in outcomes and predictors of all-cause mortality after percutaneous coronary intervention (Data from United Kingdom and Sweden). Am J Cardiol. 2017;119(2):210–6. https://doi.org/10.1016/j.amjcard.2016.09.052.

    PubMed  Article  Google Scholar 

  10. Boden WE, O’Rourke RA, Teo KK, Hartigan PM, Maron DJ, Kostuk WJ, et al. Optimal medical therapy with or without PCI for stable coronary disease. N Engl J Med. 2007;356(15):1503–16. https://doi.org/10.1056/NEJMoa070829.

    PubMed  CAS  Article  Google Scholar 

  11. Al-Lamee R, Thompson D, Dehbi HM, Sen S, Tang K, Davies J, et al. Percutaneous coronary intervention in stable angina (ORBITA): a double-blind, randomised controlled trial. Lancet (London, England). 2018;391(10115):31–40. https://doi.org/10.1016/s0140-6736(17)32714-9.

    Article  Google Scholar 

  12. Amsterdam EA, Wenger NK, Brindis RG, Casey DE Jr, Ganiats TG, Holmes DR Jr, et al. 2014 AHA/ACC guideline for the management of patients with non-ST-elevation acute coronary syndromes: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol. 2014;64(24):e139–228. https://doi.org/10.1016/j.jacc.2014.09.017.

    PubMed  Article  Google Scholar 

  13. O’Gara PT, Kushner FG, Ascheim DD, Casey DE Jr, Chung MK, de Lemos JA, et al. 2013 ACCF/AHA guideline for the management of ST-elevation myocardial infarction: executive summary: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines: developed in collaboration with the American College of Emergency Physicians and Society for Cardiovascular Angiography and Interventions. Cathet Cardiovasc Interv. 2013;82(1):E1–27. https://doi.org/10.1002/ccd.24776.

    Article  Google Scholar 

  14. NICE Guidelines CG 172. November 2013. MI—secondary prevention: Secondary prevention in primary and secondary care for patients following a myocardial infarction. https://www.nice.org.uk/guidance/cg48. Accessed 13 Sept 2017.

  15. Yonetsu T, Kakuta T, Lee T, Takayama K, Kakita K, Iwamoto T, et al. Assessment of acute injuries and chronic intimal thickening of the radial artery after transradial coronary intervention by optical coherence tomography. Eur Heart J. 2010;31(13):1608–15. https://doi.org/10.1093/eurheartj/ehq102.

    PubMed  Article  Google Scholar 

  16. Dawson EA, Rathore S, Cable NT, Wright DJ, Morris JL, Green DJ. Impact of introducer sheath coating on endothelial function in humans after transradial coronary procedures. Circ Cardiovasc Interv. 2010;3(2):148–56. https://doi.org/10.1161/circinterventions.109.912022.

    PubMed  Article  Google Scholar 

  17. Mitchell A, Fujisawa T, Mills NL, Brittan M, Newby DE, Cruden NLM. Endothelial progenitor cell biology and vascular recovery following transradial cardiac catheterization. J Am Heart Assoc. 2017. https://doi.org/10.1161/jaha.117.006610.

    PubMed  PubMed Central  Article  Google Scholar 

  18. Armstrong PW. A comparison of pharmacologic therapy with/without timely coronary intervention vs. primary percutaneous intervention early after ST-elevation myocardial infarction: the WEST (Which EARLY ST-elevation myocardial infarction Therapy) study. Eur Heart J. 2006;27(13):1530–8. https://doi.org/10.1093/eurheartj/ehl088.

    PubMed  Article  Google Scholar 

  19. Palmerini T, Serruys P, Kappetein AP, Genereux P, Riva DD, Reggiani LB, et al. Clinical outcomes with percutaneous coronary revascularization vs coronary artery bypass grafting surgery in patients with unprotected left main coronary artery disease: A meta-analysis of 6 randomized trials and 4,686 patients. Am Heart J. 2017;190:54–63. https://doi.org/10.1016/j.ahj.2017.05.005.

    PubMed  Article  Google Scholar 

  20. Kerr A, Williams MJ, White H, Grey C, Jiang Y, Nunn C. 30-day mortality after percutaneous coronary intervention in New Zealand public hospitals (ANZACS-QI 18). N Zeal Med J. 2017;130(1459):54–63.

    Google Scholar 

  21. McDonald AI, Iruela-Arispe ML. Healing arterial ulcers: Endothelial lining regeneration upon vascular denudation injury. Vasc Pharmacol. 2015;72:9–15. https://doi.org/10.1016/j.vph.2015.06.007.

    CAS  Article  Google Scholar 

  22. Otsuka F, Finn AV, Yazdani SK, Nakano M, Kolodgie FD, Virmani R. The importance of the endothelium in atherothrombosis and coronary stenting. Nat Rev Cardiol. 2012;9(8):439–53. https://doi.org/10.1038/nrcardio.2012.64.

    PubMed  CAS  Article  Google Scholar 

  23. Kipshidze N, Dangas G, Tsapenko M, Moses J, Leon MB, Kutryk M, et al. Role of the endothelium in modulating neointimal formation: vasculoprotective approaches to attenuate restenosis after percutaneous coronary interventions. J Am Coll Cardiol. 2004;44(4):733–9. https://doi.org/10.1016/j.jacc.2004.04.048.

    PubMed  CAS  Article  Google Scholar 

  24. Hadoke P, Wainwright CL, Wadsworth RM, Butler K, Giddings MJ. Characterization of the morphological and functional alterations in rabbit subclavian artery subjected to balloon angioplasty. Coron Artery Dis. 1995;6(5):403–15.

    PubMed  CAS  Article  Google Scholar 

  25. Plass CA, Sabdyusheva-Litschauer I, Bernhart A, Samaha E, Petnehazy O, Szentirmai E, et al. Time course of endothelium-dependent and -independent coronary vasomotor response to coronary balloons and stents. Comparison of plain and drug-eluting balloons and stents. JACC Cardiovasc Interv. 2012;5(7):741–51. https://doi.org/10.1016/j.jcin.2012.03.021.

    PubMed  Article  Google Scholar 

  26. Ip JH, Fuster V, Badimon L, Badimon J, Taubman MB, Chesebro JH. Syndromes of accelerated atherosclerosis: role of vascular injury and smooth muscle cell proliferation. J Am Coll Cardiol. 1990;15(7):1667–87.

    PubMed  CAS  Article  Google Scholar 

  27. Fingerle J, Au YP, Clowes AW, Reidy MA. Intimal lesion formation in rat carotid arteries after endothelial denudation in absence of medial injury. Arteriosclerosis (Dallas, Tex). 1990;10(6):1082–7.

    CAS  Google Scholar 

  28. Bjorkerud S, Bondjers G. Arterial repair and atherosclerosis after mechanical injury. 5. Tissue response after induction of a large superficial transverse injury. Atherosclerosis. 1973;18(2):235–55.

    PubMed  CAS  Article  Google Scholar 

  29. Pendyala L, Yin X, Li J, Shinke T, Xu Y, Chen JP, et al. Polymer-free cerivastatin-eluting stent shows superior neointimal inhibition with preserved vasomotor function compared to polymer-based paclitaxel-eluting stent in rabbit iliac arteries. EuroIntervention J EuroPCR Collab Work Group Interv Cardiol Eur Soc Cardiol. 2010;6(1):126–33.

    Google Scholar 

  30. Sarno G, Lagerqvist B, Frobert O, Nilsson J, Olivecrona G, Omerovic E, et al. Lower risk of stent thrombosis and restenosis with unrestricted use of ‘new-generation’ drug-eluting stents: a report from the nationwide Swedish Coronary Angiography and Angioplasty Registry (SCAAR). Eur Heart J. 2012;33(5):606–13. https://doi.org/10.1093/eurheartj/ehr479.

    PubMed  Article  Google Scholar 

  31. Qian F, Zhong Y, Hannan EL. Four-year comparative effectiveness of bare-metal and everolimus-eluting stents in New York. Catheter Cardiovasc Interv. 2017. https://doi.org/10.1002/ccd.27144.

    PubMed  Article  Google Scholar 

  32. Kirtane AJ, Gupta A, Iyengar S, Moses JW, Leon MB, Applegate R, et al. Safety and efficacy of drug-eluting and bare metal stents: comprehensive meta-analysis of randomized trials and observational studies. Circulation. 2009;119(25):3198–206. https://doi.org/10.1161/circulationaha.108.826479.

    PubMed  CAS  Article  Google Scholar 

  33. Sabbah M, Kadota K, El-Eraky A, Kamal HM, Abdellah AT, El Hawary A. Comparison of in-stent neoatherosclerosis and tissue characteristics between early and late in-stent restenosis in second-generation drug-eluting stents: an optical coherence tomography study. Int J Cardiovasc Imaging. 2017. https://doi.org/10.1007/s10554-017-1146-7.

    PubMed  Article  Google Scholar 

  34. Farooq V, Gogas BD, Serruys PW. Restenosis: delineating the numerous causes of drug-eluting stent restenosis. Circ Cardiovasc Interv. 2011;4(2):195–205. https://doi.org/10.1161/circinterventions.110.959882.

    PubMed  Article  Google Scholar 

  35. Stettler C, Wandel S, Allemann S, Kastrati A, Morice MC, Schomig A, et al. Outcomes associated with drug-eluting and bare-metal stents: a collaborative network meta-analysis. Lancet (London, England). 2007;370(9591):937–48. https://doi.org/10.1016/s0140-6736(07)61444-5.

    CAS  Article  Google Scholar 

  36. Mauri L, Hsieh WH, Massaro JM, Ho KK, D’Agostino R, Cutlip DE. Stent thrombosis in randomized clinical trials of drug-eluting stents. N Engl J Med. 2007;356(10):1020–9. https://doi.org/10.1056/NEJMoa067731.

    PubMed  CAS  Article  Google Scholar 

  37. Wu X, Zhao Y, Tang C, Yin T, Du R, Tian J, et al. Re-endothelialization study on endovascular stents seeded by endothelial cells through up- or downregulation of VEGF. ACS Appl Mater Interfaces. 2016;8(11):7578–89. https://doi.org/10.1021/acsami.6b00152.

    PubMed  CAS  Article  Google Scholar 

  38. Choi WG, Kim SH, Yoon HS, Lee EJ, Kim DW. Impact of an endothelial progenitor cell capturing stent on coronary microvascular function: comparison with drug-eluting stents. Korean J Intern Med. 2015;30(1):42–8. https://doi.org/10.3904/kjim.2015.30.1.42.

    PubMed  Article  Google Scholar 

  39. Sandhu K, Butler R, Nolan J. Expert opinion: transradial coronary artery procedures: tips for success. Interv Cardiol (Lond, Engl). 2017;12(1):18–24. https://doi.org/10.15420/icr.2017:2:2.

    Article  Google Scholar 

  40. Barry MM, Foulon P, Touati G, Ledoux B, Sevestre H, Carmi D, et al. Comparative histological and biometric study of the coronary, radial and left internal thoracic arteries. Surg Radiol Anat SRA. 2003;25(3–4):284–9. https://doi.org/10.1007/s00276-003-0142-x.

    PubMed  CAS  Article  Google Scholar 

  41. Zhenxian Y, Yujie Z, Yingxin Z, Zhiming Z, Shiwei Y, Zhijian W. Impact of transradial coronary procedures on radial artery. Angiology. 2010;61(1):8–13. https://doi.org/10.1177/0003319709348293.

    Article  Google Scholar 

  42. Nagai S, Abe S, Sato T, Hozawa K, Yuki K, Hanashima K, et al. Ultrasonic assessment of vascular complications in coronary angiography and angioplasty after transradial approach. Am J Cardiol. 1999;83(2):180–6.

    PubMed  CAS  Article  Google Scholar 

  43. Adingupu DD, Westergren HU, Dahgam S, Jonsson-Rylander AC, Blomster J, Albertsson P, et al. Radial artery intima-media thickness regresses after secondary prevention interventions in patients’ post-acute coronary syndrome and is associated with cardiac and kidney biomarkers. Oncotarget. 2017;8(32):53419–31. https://doi.org/10.18632/oncotarget.18511.

    PubMed  PubMed Central  Article  Google Scholar 

  44. Thijssen DH, Scholten RR, van den Munckhof IC, Benda N, Green DJ, Hopman MT. Acute change in vascular tone alters intima-media thickness. Hypertension (Dallas, Tex: 1979). 2011;58(2):240–6. https://doi.org/10.1161/hypertensionaha.111.173583.

    CAS  Article  Google Scholar 

  45. Wakeyama T, Ogawa H, Iida H, Takaki A, Iwami T, Mochizuki M, et al. Intima-media thickening of the radial artery after transradial intervention. An intravascular ultrasound study. J Am Coll Cardiol. 2003;41(7):1109–14.

    PubMed  Article  Google Scholar 

  46. Kamiya H, Ushijima T, Kanamori T, Ikeda C, Nakagaki C, Ueyama K, et al. Use of the radial artery graft after transradial catheterization: is it suitable as a bypass conduit? Ann Thorac Surg. 2003;76(5):1505–9.

    PubMed  Article  Google Scholar 

  47. Green DJ, Hopman MT, Padilla J, Laughlin MH, Thijssen DH. Vascular adaptation to exercise in humans: role of hemodynamic stimuli. Physiol Rev. 2017;97(2):495–528. https://doi.org/10.1152/physrev.00014.2016.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  48. Weidinger FF, McLenachan JM, Cybulsky MI, Gordon JB, Rennke HG, Hollenberg NK, et al. Persistent dysfunction of regenerated endothelium after balloon angioplasty of rabbit iliac artery. Circulation. 1990;81(5):1667–79.

    PubMed  CAS  Article  Google Scholar 

  49. Kitta Y, Nakamura T, Kodama Y, Takano H, Umetani K, Fujioka D, et al. Endothelial vasomotor dysfunction in the brachial artery is associated with late in-stent coronary restenosis. J Am Coll Cardiol. 2005;46(4):648–55. https://doi.org/10.1016/j.jacc.2005.04.055.

    PubMed  Article  Google Scholar 

  50. Strotmann JM, Bauersachs J, Fraccarollo D, Kirchengast M, Schnabel PA, Sykora J, et al. Trauma induced by nontraumatic coronary devices and its impact on vascular reactivity and morphology. Am J Physiol Heart Circ Physiol. 2002;283(6):H2356–62. https://doi.org/10.1152/ajpheart.00402.2002.

    PubMed  CAS  Article  Google Scholar 

  51. Fonseca FA, Izar MC, Fuster V, Gallo R, Padurean A, Fallon JT, et al. Chronic endothelial dysfunction after oversized coronary balloon angioplasty in pigs: a 12-week follow-up of coronary vasoreactivity in vivo and in vitro. Atherosclerosis. 2001;154(1):61–9.

    PubMed  CAS  Article  Google Scholar 

  52. Lamping KG, Marcus ML, Dole WP. Removal of the endothelium potentiates canine large coronary artery constrictor responses to 5-hydroxytryptamine in vivo. Circ Res. 1985;57(1):46–54.

    PubMed  CAS  Article  Google Scholar 

  53. Mc Fadden EP, Bauters C, Lablanche JM, Quandalle P, Leroy F, Bertrand ME. Response of human coronary arteries to serotonin after injury by coronary angioplasty. Circulation. 1993;88(5 Pt 1):2076–85.

    PubMed  CAS  Article  Google Scholar 

  54. Berdeaux A, Ghaleh B, Dubois-Rande JL, Vigue B, Drieu La Rochelle C, Hittinger L, et al. Role of vascular endothelium in exercise-induced dilation of large epicardial coronary arteries in conscious dogs. Circulation. 1994;89(6):2799–808.

    PubMed  CAS  Article  Google Scholar 

  55. Jerius H, Bagwell D, Beall A, Brophy C. The impact of balloon embolectomy on the function and morphology of the endothelium. J Surg Res. 1997;67(1):9–13. https://doi.org/10.1006/jsre.1996.4908.

    PubMed  CAS  Article  Google Scholar 

  56. Saitoh S, Saito T, Ohwada T, Ohtake A, Onogi F, Aikawa K, et al. Morphological and functional changes in coronary vessel evoked by repeated endothelial injury in pigs. Cardiovasc Res. 1998;38(3):772–81.

    PubMed  CAS  Article  Google Scholar 

  57. Cartier R, Pearson PJ, Lin PJ, Schaff HV. Time course and extent of recovery of endothelium-dependent contractions and relaxations after direct arterial injury. J Thorac Cardiovasc Surg. 1991;102(3):371–7.

    PubMed  CAS  Google Scholar 

  58. Pohl U, Holtz J, Busse R, Bassenge E. Crucial role of endothelium in the vasodilator response to increased flow in vivo. Hypertension (Dallas, Tex: 1979). 1986;8(1):37–44.

    CAS  Article  Google Scholar 

  59. Dawson EA, Rathore S, Cable NT, Wright DJ, Morris JL, Green DJ. Impact of catheter insertion using the radial approach on vasodilatation in humans. Clin Sci (London, England: 1979). 2010;118(10):633–40. https://doi.org/10.1042/cs20090548.

    Article  Google Scholar 

  60. Burstein JM, Gidrewicz D, Hutchison SJ, Holmes K, Jolly S, Cantor WJ. Impact of radial artery cannulation for coronary angiography and angioplasty on radial artery function. Am J Cardiol. 2007;99(4):457–9. https://doi.org/10.1016/j.amjcard.2006.08.055.

    PubMed  Article  Google Scholar 

  61. Horigome M, Kumazaki S, Hattori N, Kasai H, Horigome M, Aizawa K, et al. Noninvasive evaluation of coronary endothelial function following sirolimus-eluting stent implantation by using positron emission tomography. Cardiology. 2009;114(3):157–63. https://doi.org/10.1159/000226093.

    PubMed  CAS  Article  Google Scholar 

  62. Pendyala LK, Matsumoto D, Shinke T, Iwasaki T, Sugimoto R, Hou D, et al. Nobori stent shows less vascular inflammation and early recovery of endothelial function compared with Cypher stent. JACC Cardiovasc Interv. 2012;5(4):436–44. https://doi.org/10.1016/j.jcin.2011.11.013.

    PubMed  Article  Google Scholar 

  63. Gogas BD, Benham JJ, Hsu S, Sheehy A, Lefer DJ, Goodchild TT, et al. Vasomotor function comparative assessment at 1 and 2 years following implantation of the absorb everolimus-eluting bioresorbable vascular scaffold and the xience V everolimus-eluting metallic stent in porcine coronary arteries: insights from in vivo angiography, ex vivo assessment, and gene analysis at the stented/scaffolded segments and the proximal and distal edges. JACC Cardiovasc Interv. 2016;9(7):728–41. https://doi.org/10.1016/j.jcin.2015.12.018.

    PubMed  Article  Google Scholar 

  64. Hamilos M, Ribichini F, Ostojic MC, Ferrero V, Orlic D, Vassanelli C, et al. Coronary vasomotion one year after drug-eluting stent implantation: comparison of everolimus-eluting and paclitaxel-eluting coronary stents. J Cardiovasc Transl Res. 2014;7(4):406–12. https://doi.org/10.1007/s12265-014-9568-2.

    PubMed  Article  Google Scholar 

  65. Kim JW, Seo HS, Park JH, Na JO, Choi CU, Lim HE, et al. A prospective, randomized, 6-month comparison of the coronary vasomotor response associated with a zotarolimus- versus a sirolimus-eluting stent: differential recovery of coronary endothelial dysfunction. J Am Coll Cardiol. 2009;53(18):1653–9. https://doi.org/10.1016/j.jacc.2009.01.051.

    PubMed  CAS  Article  Google Scholar 

  66. Hamilos MI, Ostojic M, Beleslin B, Sagic D, Mangovski L, Stojkovic S, et al. Differential effects of drug-eluting stents on local endothelium-dependent coronary vasomotion. J Am Coll Cardiol. 2008;51(22):2123–9. https://doi.org/10.1016/j.jacc.2007.12.059.

    PubMed  CAS  Article  Google Scholar 

  67. Mitsutake Y, Ueno T, Yokoyama S, Sasaki K, Sugi Y, Toyama Y, et al. Coronary endothelial dysfunction distal to stent of first-generation drug-eluting stents. JACC Cardiovasc Interv. 2012;5(9):966–73. https://doi.org/10.1016/j.jcin.2012.06.010.

    PubMed  Article  Google Scholar 

  68. Mitsutake Y, Ueno T, Ikeno F, Yokoyama S, Sasaki K, Nakayoshi T, et al. Serial changes of coronary endothelial function and arterial healing after paclitaxel-eluting stent implantation. Cardiovasc Interv Ther. 2016;31(1):21–8. https://doi.org/10.1007/s12928-015-0341-5.

    PubMed  CAS  Article  Google Scholar 

  69. Li J, Jabara R, Pendyala L, Otsuka Y, Shinke T, Hou D, et al. Abnormal vasomotor function of porcine coronary arteries distal to sirolimus-eluting stents. JACC Cardiovasc Interv. 2008;1(3):279–85. https://doi.org/10.1016/j.jcin.2008.01.009.

    PubMed  CAS  Article  Google Scholar 

  70. Yan Z, Zhou Y, Zhao Y, Zhou Z, Yang S, Wang Z. Impact of transradial coronary procedures on radial artery function. Angiology. 2014;65(2):104–7. https://doi.org/10.1177/0003319713479650.

    PubMed  Article  Google Scholar 

  71. Madssen E, Haere P, Wiseth R. Radial artery diameter and vasodilatory properties after transradial coronary angiography. Ann Thorac Surg. 2006;82(5):1698–702. https://doi.org/10.1016/j.athoracsur.2006.06.017.

    PubMed  Article  Google Scholar 

  72. De Vita A, Milo M, Sestito A, Lamendola P, Lanza GA, Crea F. Association of coronary microvascular dysfunction with restenosis of left anterior descending coronary artery disease treated by percutaneous intervention. Int J Cardiol. 2016;219:322–5. https://doi.org/10.1016/j.ijcard.2016.06.031.

    PubMed  Article  Google Scholar 

  73. Dawson EA, Alkarmi A, Thijssen DH, Rathore S, Marsman DE, Cable NT, et al. Low-flow mediated constriction is endothelium-dependent: effects of exercise training after radial artery catheterization. Circ Cardiovasc Interv. 2012;5(5):713–9. https://doi.org/10.1161/circinterventions.112.971556.

    PubMed  Article  Google Scholar 

  74. Patti G, Pasceri V, Melfi R, Goffredo C, Chello M, D’Ambrosio A, et al. Impaired flow-mediated dilation and risk of restenosis in patients undergoing coronary stent implantation. Circulation. 2005;111(1):70–5. https://doi.org/10.1161/01.cir.0000151308.06673.d2.

    PubMed  Article  Google Scholar 

  75. Akcakoyun M, Kargin R, Tanalp AC, Pala S, Ozveren O, Akcay M, et al. Predictive value of noninvasively determined endothelial dysfunction for long-term cardiovascular events and restenosis in patients undergoing coronary stent implantation: a prospective study. Coron Artery Dis. 2008;19(5):337–43. https://doi.org/10.1097/MCA.0b013e328301ba8e.

    PubMed  Article  Google Scholar 

  76. Mizia-Stec K, Gasior Z, Haberka M, Mizia M, Chmiel A, Janowska J, et al. In-stent coronary restenosis, but not the type of stent, is associated with impaired endothelial-dependent vasodilatation. Kardiologia polska. 2009;67(1):9–17 (discussion 8).

    PubMed  Google Scholar 

  77. Halcox JP, Schenke WH, Zalos G, Mincemoyer R, Prasad A, Waclawiw MA, et al. Prognostic value of coronary vascular endothelial dysfunction. Circulation. 2002;106(6):653–8.

    PubMed  Article  Google Scholar 

  78. Inaba Y, Chen JA, Bergmann SR. Prediction of future cardiovascular outcomes by flow-mediated vasodilatation of brachial artery: a meta-analysis. Int J Cardiovasc Imaging. 2010;26(6):631–40. https://doi.org/10.1007/s10554-010-9616-1.

    PubMed  Article  Google Scholar 

  79. Ras RT, Streppel MT, Draijer R, Zock PL. Flow-mediated dilation and cardiovascular risk prediction: a systematic review with meta-analysis. Int J Cardiol. 2013;168(1):344–51. https://doi.org/10.1016/j.ijcard.2012.09.047.

    PubMed  Article  Google Scholar 

  80. Kubo M, Miyoshi T, Oe H, Ohno Y, Nakamura K, Ito H. Prognostic significance of endothelial dysfunction in patients undergoing percutaneous coronary intervention in the era of drug-eluting stents. BMC Cardiovasc Disord. 2015;15:102. https://doi.org/10.1186/s12872-015-0096-z.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  81. Ribeiro L, de Assuncao e Silva F, Kurihara RS, Schor N, Mieko E, Higa S. Evaluation of the nitric oxide production in rat renal artery smooth muscle cells culture exposed to radiocontrast agents. Kidney Int. 2004;65(2):589–96. https://doi.org/10.1111/j.1523-1755.2004.00408.x.

    PubMed  CAS  Article  Google Scholar 

  82. Zelis R, Caudill CC, Baggette K, Mason DT. Reflex vasodilation induced by coronary angiography in human subjects. Circulation. 1976;53(3):490–3.

    PubMed  CAS  Article  Google Scholar 

  83. Limbruno U, Petronio AS, Amoroso G, Baglini R, Paterni G, Merelli A, et al. The impact of coronary artery disease on the coronary vasomotor response to nonionic contrast media. Circulation. 2000;101(5):491–7.

    PubMed  CAS  Article  Google Scholar 

  84. Satoh A, Matsuda Y, Sakai H, Nakatsuka M, Ogawa H, Katayama K, et al. Coronary artery spasm during cardiac angiography. Clin Cardiol. 1990;13(1):55–8.

    PubMed  CAS  Article  Google Scholar 

  85. Barstad RM, Buchmann MS, Hamers MJ, Orning L, Orvim U, Stormorken H, et al. Effects of ionic and nonionic contrast media on endothelium and on arterial thrombus formation. Acta Radiol (Stockholm, Sweden: 1987). 1996;37(6):954–61. https://doi.org/10.1177/02841851960373p2102.

    CAS  Article  Google Scholar 

  86. Kaessmeyer S, Sehl J, Khiao In M, Hiebl B, Merle R, Jung F, et al. Organotypic soft-tissue co-cultures: morphological changes in microvascular endothelial tubes after incubation with iodinated contrast media. Clin Hemorheol Microcirc. 2016;64(3):391–402. https://doi.org/10.3233/ch-168119.

    PubMed  CAS  Article  Google Scholar 

  87. Wang YX, Chan P, Morcos SK. The effect of radiographic contrast media on human vascular smooth muscle cells. Br J Radiol. 1998;71(844):376–80. https://doi.org/10.1259/bjr.71.844.9659129.

    PubMed  CAS  Article  Google Scholar 

  88. Takatsuki H, Furukawa T, Liu Y, Hirano K, Yoshikoshi A, Sakanishi A. Effect of contrast media on vascular smooth muscle cells. Acta Radiol (Stockholm, Sweden: 1987). 2004;45(6):635–40.

    CAS  Google Scholar 

  89. Gomi N. Vasoconstriction by angiographic contrast media in isolated canine arteries. Br J Radiol. 1992;65(779):961–7. https://doi.org/10.1259/0007-1285-65-779-961.

    PubMed  CAS  Article  Google Scholar 

  90. Kelly RV, Gillespie MJ, Cohen MG, McLaughlin DP, Magnus Ohman E, Stouffer GA. The contrast media iohexol causes vasoconstriction of the proximal left anterior descending coronary artery: implications for appropriate stent sizing. Angiology. 2008;59(5):574–80. https://doi.org/10.1177/0003319708318375.

    PubMed  Article  Google Scholar 

  91. Karstoft J, Baath L, Jansen I, Edvinsson L. Vasoconstriction of isolated arteries induced by angiographic contrast media. A comparison of ionic and non-ionic contrast media iso-osmolar with plasma. Acta Radiol (Stockholm, Sweden: 1987). 1995;36(3):312–6.

    CAS  Google Scholar 

  92. Giedrojc J, Radziwon P, Krupinski K, Kielpinska K, Galar M, Bielawiec M. Effect of nonionic and ionic contrast media on fibrinolysis in patients undergoing angiography. Pol J Pharmacol. 1996;48(3):323–6.

    PubMed  CAS  Article  Google Scholar 

  93. Xiang L, Xiang G, Zhang J, Yue L, Zhao L. Contrast agent suppresses endothelium-dependent arterial dilation after digital subtraction angiography procedure in patients with diabetic foot. Endocrine. 2014;46(3):505–11. https://doi.org/10.1007/s12020-013-0095-8.

    PubMed  CAS  Article  Google Scholar 

  94. Genovesi E, Romanello M, De Caterina R. Contrast-induced acute kidney injury in cardiology. Giornale italiano di cardiologia (2006). 2016;17(12):984–1000. https://doi.org/10.1714/2612.26891.

    Article  Google Scholar 

  95. Cao S, Wang P, Cui K, Zhang L, Hou Y. Atorvastatin prevents contrast agent-induced renal injury in patients undergoing coronary angiography by inhibiting oxidative stress. Nan fang yi ke da xue xue bao = J South Med Univ. 2012;32(11):1600–2.

    CAS  Google Scholar 

  96. Chiang CH, Huang PH, Chiu CC, Hsu CY, Leu HB, Huang CC, et al. Reduction of circulating endothelial progenitor cell level is associated with contrast-induced nephropathy in patients undergoing percutaneous coronary and peripheral interventions. PLoS One. 2014;9(3):e89942. https://doi.org/10.1371/journal.pone.0089942.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  97. Mehran R, Aymong ED, Nikolsky E, Lasic Z, Iakovou I, Fahy M, et al. A simple risk score for prediction of contrast-induced nephropathy after percutaneous coronary intervention: development and initial validation. J Am Coll Cardiol. 2004;44(7):1393–9. https://doi.org/10.1016/j.jacc.2004.06.068.

    PubMed  Article  Google Scholar 

  98. Azevedo LC, Pedro MA, Souza LC, de Souza HP, Janiszewski M, da Luz PL, et al. Oxidative stress as a signaling mechanism of the vascular response to injury: the redox hypothesis of restenosis. Cardiovasc Res. 2000;47(3):436–45.

    PubMed  CAS  Article  Google Scholar 

  99. Juni RP, Duckers HJ, Vanhoutte PM, Virmani R, Moens AL. Oxidative stress and pathological changes after coronary artery interventions. J Am Coll Cardiol. 2013;61(14):1471–81. https://doi.org/10.1016/j.jacc.2012.11.068.

    PubMed  CAS  Article  Google Scholar 

  100. Shi Y, Niculescu R, Wang D, Patel S, Davenpeck KL, Zalewski A. Increased NAD(P)H oxidase and reactive oxygen species in coronary arteries after balloon injury. Arterioscler Thromb Vasc Biol. 2001;21(5):739–45.

    PubMed  CAS  Article  Google Scholar 

  101. Tsimikas S, Lau HK, Han KR, Shortal B, Miller ER, Segev A, et al. Percutaneous coronary intervention results in acute increases in oxidized phospholipids and lipoprotein(a): short-term and long-term immunologic responses to oxidized low-density lipoprotein. Circulation. 2004;109(25):3164–70. https://doi.org/10.1161/01.cir.0000130844.01174.55.

    PubMed  CAS  Article  Google Scholar 

  102. Berg K, Wiseth R, Bjerve K, Brurok H, Gunnes S, Skarra S, et al. Oxidative stress and myocardial damage during elective percutaneous coronary interventions and coronary angiography. A comparison of blood-borne isoprostane and troponin release. Free Radic Res. 2004;38(5):517–25.

    PubMed  CAS  Article  Google Scholar 

  103. Pendyala LK, Li J, Shinke T, Geva S, Yin X, Chen JP, et al. Endothelium-dependent vasomotor dysfunction in pig coronary arteries with Paclitaxel-eluting stents is associated with inflammation and oxidative stress. JACC Cardiovasc Interv. 2009;2(3):253–62. https://doi.org/10.1016/j.jcin.2008.11.009.

    PubMed  Article  Google Scholar 

  104. Nunes GL, Robinson K, Kalynych A, King SB 3rd, Sgoutas DS, Berk BC. Vitamins C and E inhibit O2-production in the pig coronary artery. Circulation. 1997;96(10):3593–601.

    PubMed  CAS  Article  Google Scholar 

  105. Blum A, Schneider DJ, Sobel BE, Dauerman HL. Endothelial dysfunction and inflammation after percutaneous coronary intervention. Am J Cardiol. 2004;94(11):1420–3. https://doi.org/10.1016/j.amjcard.2004.07.146.

    PubMed  CAS  Article  Google Scholar 

  106. Majesky MW, Reidy MA, Bowen-Pope DF, Hart CE, Wilcox JN, Schwartz SM. PDGF ligand and receptor gene expression during repair of arterial injury. J Cell Biol. 1990;111(5 Pt 1):2149–58.

    PubMed  CAS  Article  Google Scholar 

  107. Barbato JE, Tzeng E. Nitric oxide and arterial disease. J Vasc Surg. 2004;40(1):187–93. https://doi.org/10.1016/j.jvs.2004.03.043.

    PubMed  Article  Google Scholar 

  108. Pasternak RC, Baughman KL, Fallon JT, Block PC. Scanning electron microscopy after coronary transluminal angioplasty of normal canine coronary arteries. Am J Cardiol. 1980;45(3):591–8.

    PubMed  CAS  Article  Google Scholar 

  109. Jeremy JY, Rowe D, Emsley AM, Newby AC. Nitric oxide and the proliferation of vascular smooth muscle cells. Cardiovasc Res. 1999;43(3):580–94.

    PubMed  CAS  Article  Google Scholar 

  110. Sundaresan M, Yu ZX, Ferrans VJ, Irani K, Finkel T. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science (New York, NY). 1995;270(5234):296–9.

    CAS  Article  Google Scholar 

  111. Bai H, Masuda J, Sawa Y, Nakano S, Shirakura R, Shimazaki Y, et al. Neointima formation after vascular stent implantation. Spatial and chronological distribution of smooth muscle cell proliferation and phenotypic modulation. Arterioscler Thromb J Vasc Biol. 1994;14(11):1846–53.

    CAS  Article  Google Scholar 

  112. Gong KW, Zhu GY, Wang LH, Tang CS. Effect of active oxygen species on intimal proliferation in rat aorta after arterial injury. J Vasc Res. 1996;33(1):42–6.

    PubMed  CAS  Article  Google Scholar 

  113. Szocs K, Lassegue B, Sorescu D, Hilenski LL, Valppu L, Couse TL, et al. Upregulation of Nox-based NAD(P)H oxidases in restenosis after carotid injury. Arterioscler Thromb Vasc Biol. 2002;22(1):21–7.

    PubMed  CAS  Article  Google Scholar 

  114. Kochiadakis GE, Arfanakis DA, Marketou ME, Skalidis EI, Igoumenidis NE, Nikitovic D, et al. Oxidative stress changes after stent implantation: a randomized comparative study of sirolimus-eluting and bare metal stents. Int J Cardiol. 2010;142(1):33–7. https://doi.org/10.1016/j.ijcard.2008.12.105.

    PubMed  Article  Google Scholar 

  115. Di Serafino L, Sarma J, Dierickx K, Ntarladimas I, Pyxaras SA, Delrue L, et al. Monocyte-platelets aggregates as cellular biomarker of endothelium-dependent coronary vasomotor dysfunction in patients with coronary artery disease. J Cardiovasc Transl Res. 2014;7(1):1–8. https://doi.org/10.1007/s12265-013-9520-x.

    PubMed  Article  Google Scholar 

  116. Liang D, Zhang Q, Yang H, Zhang R, Yan W, Gao H, et al. Anti-oxidative stress effect of loading-dose rosuvastatin prior to percutaneous coronary intervention in patients with acute coronary syndrome: a prospective randomized controlled clinical trial. Clin Drug Investig. 2014;34(11):773–81. https://doi.org/10.1007/s40261-014-0231-0.

    PubMed  CAS  Article  Google Scholar 

  117. Freyschuss A, Stiko-Rahm A, Swedenborg J, Henriksson P, Bjorkhem I, Berglund L, et al. Antioxidant treatment inhibits the development of intimal thickening after balloon injury of the aorta in hypercholesterolemic rabbits. J Clin Investig. 1993;91(4):1282–8. https://doi.org/10.1172/jci116326.

    PubMed  CAS  Article  PubMed Central  Google Scholar 

  118. Liu J, Li M, Lu H, Qiao W, Xi D, Luo T, et al. Effects of probucol on restenosis after percutaneous coronary intervention: a systematic review and meta-analysis. PLoS One. 2015;10(4):e0124021. https://doi.org/10.1371/journal.pone.0124021.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  119. Tardif JC, Gregoire J, Schwartz L, Title L, Laramee L, Reeves F, et al. Effects of AGI-1067 and probucol after percutaneous coronary interventions. Circulation. 2003;107(4):552–8.

    PubMed  CAS  Article  Google Scholar 

  120. Abe N, Kashima Y, Izawa A, Motoki H, Ebisawa S, Miyashita Y, et al. A 2-year follow-up of oxidative stress levels in patients with ST-segment elevation myocardial infarction: a subanalysis of the ALPS-AMI study. Angiology. 2015;66(3):271–7. https://doi.org/10.1177/0003319714525656.

    PubMed  Article  Google Scholar 

  121. Walter DH, Rittig K, Bahlmann FH, Kirchmair R, Silver M, Murayama T, et al. Statin therapy accelerates reendothelialization: a novel effect involving mobilization and incorporation of bone marrow-derived endothelial progenitor cells. Circulation. 2002;105(25):3017–24.

    PubMed  CAS  Article  Google Scholar 

  122. Iwakura A, Luedemann C, Shastry S, Hanley A, Kearney M, Aikawa R, et al. Estrogen-mediated, endothelial nitric oxide synthase-dependent mobilization of bone marrow-derived endothelial progenitor cells contributes to reendothelialization after arterial injury. Circulation. 2003;108(25):3115–21. https://doi.org/10.1161/01.cir.0000106906.56972.83.

    PubMed  CAS  Article  Google Scholar 

  123. Lin HH, Chen YH, Yet SF, Chau LY. After vascular injury, heme oxygenase-1/carbon monoxide enhances re-endothelialization via promoting mobilization of circulating endothelial progenitor cells. J Thromb Haemost JTH. 2009;7(8):1401–8. https://doi.org/10.1111/j.1538-7836.2009.03478.x.

    PubMed  CAS  Article  Google Scholar 

  124. Werner N, Priller J, Laufs U, Endres M, Bohm M, Dirnagl U, et al. Bone marrow-derived progenitor cells modulate vascular reendothelialization and neointimal formation: effect of 3-hydroxy-3-methylglutaryl coenzyme a reductase inhibition. Arterioscler Thromb Vasc Biol. 2002;22(10):1567–72.

    PubMed  CAS  Article  Google Scholar 

  125. Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med. 2003;348(7):593–600. https://doi.org/10.1056/NEJMoa022287.

    PubMed  Article  Google Scholar 

  126. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, Technau-Ihling K, et al. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med. 2003;9(11):1370–6. https://doi.org/10.1038/nm948.

    PubMed  CAS  Article  Google Scholar 

  127. Conte MS, Choudhury RP, Shirakowa M, Fallon JT, Birinyi LK, Choudhry RP. Endothelial cell seeding fails to attenuate intimal thickening in balloon-injured rabbit arteries. J Vasc Surg. 1995;21(3):413–21.

    PubMed  CAS  Article  Google Scholar 

  128. Lan H, Wang Y, Yin T, Wang Y, Liu W, Zhang X, et al. Progress and prospects of endothelial progenitor cell therapy in coronary stent implantation. J Biomed Mater Res B Appl Biomater. 2016;104(6):1237–47. https://doi.org/10.1002/jbm.b.33398.

    PubMed  CAS  Article  Google Scholar 

  129. Schwartz SM, Haudenschild CC, Eddy EM. Endothelial regneration. I. Quantitative analysis of initial stages of endothelial regeneration in rat aortic intima. Lab Investig J Tech Methods Pathol. 1978;38(5):568–80.

    CAS  Google Scholar 

  130. Itoh Y, Toriumi H, Yamada S, Hoshino H, Suzuki N. Resident endothelial cells surrounding damaged arterial endothelium reendothelialize the lesion. Arterioscler Thromb Vasc Biol. 2010;30(9):1725–32. https://doi.org/10.1161/atvbaha.110.207365.

    PubMed  CAS  Article  Google Scholar 

  131. Hagensen MK, Raarup MK, Mortensen MB, Thim T, Nyengaard JR, Falk E, et al. Circulating endothelial progenitor cells do not contribute to regeneration of endothelium after murine arterial injury. Cardiovasc Res. 2012;93(2):223–31. https://doi.org/10.1093/cvr/cvr278.

    PubMed  CAS  Article  Google Scholar 

  132. Fishman JA, Ryan GB, Karnovsky MJ. Endothelial regeneration in the rat carotid artery and the significance of endothelial denudation in the pathogenesis of myointimal thickening. Lab Investig J Tech Methods Pathol. 1975;32(3):339–51.

    CAS  Google Scholar 

  133. Kirigaya H, Aizawa T, Ogasawara K, Sato H, Nagashima K, Onoda M, et al. Incidence of acetylcholine-induced spasm of coronary arteries subjected to balloon angioplasty. Jpn Circ J. 1993;57(9):883–90.

    PubMed  CAS  Article  Google Scholar 

  134. Finn AV, Nakazawa G, Joner M, Kolodgie FD, Mont EK, Gold HK, et al. Vascular responses to drug eluting stents: importance of delayed healing. Arterioscler Thromb Vasc Biol. 2007;27(7):1500–10. https://doi.org/10.1161/atvbaha.107.144220.

    PubMed  CAS  Article  Google Scholar 

  135. Hiasa K, Takemoto M, Matsukawa R, Matoba T, Kuga T, Sunagawa K. Chest pain without significant coronary stenosis after implantation of sirolimus-eluting stents. Intern Med (Tokyo, Japan). 2009;48(4):213–7.

    Article  Google Scholar 

  136. Won H, Kim JS, Shin DH, Kim BK, Ko YG, Choi D, et al. Relationship between endothelial vasomotor function and strut coverage after implantation of drug-eluting stent assessed by optical coherence tomography. Int J Cardiovasc Imaging. 2014;30(2):263–70. https://doi.org/10.1007/s10554-013-0325-4.

    PubMed  Article  Google Scholar 

  137. Nakata T, Fujii K, Fukunaga M, Shibuya M, Kawai K, Kawasaki D, et al. Morphological, functional, and biological vascular healing response 6 months after drug-eluting stent implantation: a randomized comparison of three drug-eluting stents. Catheter Cardiovasc Interv. 2016;88(3):350–7. https://doi.org/10.1002/ccd.26273.

    PubMed  Article  Google Scholar 

  138. Shimokawa H, Aarhus LL, Vanhoutte PM. Porcine coronary arteries with regenerated endothelium have a reduced endothelium-dependent responsiveness to aggregating platelets and serotonin. Circ Res. 1987;61(2):256–70.

    PubMed  CAS  Article  Google Scholar 

  139. Bosmans JM, Bult H, Vrints CJ, Kockx MM, Herman AG. Balloon angioplasty and induction of non-endothelial nitric oxide synthase in rabbit carotid arteries. Eur J Pharmacol. 1996;310(2–3):163–74.

    PubMed  CAS  Article  Google Scholar 

  140. Luk TH, Dai YL, Siu CW, Yiu KH, Chan HT, Lee SW, et al. Effect of exercise training on vascular endothelial function in patients with stable coronary artery disease: a randomized controlled trial. Eur J Prev Cardiol. 2012;19(4):830–9. https://doi.org/10.1177/1741826711415679.

    PubMed  Article  Google Scholar 

  141. Van Craenenbroeck EM, Frederix G, Pattyn N, Beckers P, Van Craenenbroeck AH, Gevaert A, et al. Effects of aerobic interval training and continuous training on cellular markers of endothelial integrity in coronary artery disease: a SAINTEX-CAD substudy. Am J Physiol Heart Circ Physiol. 2015;309(11):H1876–82. https://doi.org/10.1152/ajpheart.00341.2015.

    PubMed  CAS  Article  Google Scholar 

  142. Bacon SL, Sherwood A, Hinderliter A, Plourde A, Pierson L, Blumenthal JA. The influence of endothelial function and myocardial ischemia on peak oxygen consumption in patients with coronary artery disease. Int J Vasc Med. 2012;2012:274381. https://doi.org/10.1155/2012/274381.

    PubMed  PubMed Central  Article  Google Scholar 

  143. Conraads VM, Pattyn N, De Maeyer C, Beckers PJ, Coeckelberghs E, Cornelissen VA, et al. Aerobic interval training and continuous training equally improve aerobic exercise capacity in patients with coronary artery disease: the SAINTEX-CAD study. Int J Cardiol. 2015;179:203–10. https://doi.org/10.1016/j.ijcard.2014.10.155.

    PubMed  Article  Google Scholar 

  144. Mora S, Cook N, Buring JE, Ridker PM, Lee IM. Physical activity and reduced risk of cardiovascular events: potential mediating mechanisms. Circulation. 2007;116(19):2110–8. https://doi.org/10.1161/circulationaha.107.729939.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  145. Green DJ, Walsh JH, Maiorana A, Best MJ, Taylor RR, O’Driscoll JG. Exercise-induced improvement in endothelial dysfunction is not mediated by changes in CV risk factors: pooled analysis of diverse patient populations. Am J Physiol Heart Circ Physiol. 2003;285(6):H2679–87. https://doi.org/10.1152/ajpheart.00519.2003.

    PubMed  CAS  Article  Google Scholar 

  146. Joyner MJ, Green DJ. Exercise protects the cardiovascular system: effects beyond traditional risk factors. J Physiol. 2009;587(Pt 23):5551–8. https://doi.org/10.1113/jphysiol.2009.179432.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  147. Cornish AK, Broadbent S, Cheema BS. Interval training for patients with coronary artery disease: a systematic review. Eur J Appl Physiol. 2011;111(4):579–89. https://doi.org/10.1007/s00421-010-1682-5.

    PubMed  Article  Google Scholar 

  148. Cornelissen VA, Onkelinx S, Goetschalckx K, Thomaes T, Janssens S, Fagard R, et al. Exercise-based cardiac rehabilitation improves endothelial function assessed by flow-mediated dilation but not by pulse amplitude tonometry. Eur J Prev Cardiol. 2014;21(1):39–48. https://doi.org/10.1177/2047487312460516.

    PubMed  Article  Google Scholar 

  149. Gokce N, Vita JA, Bader DS, Sherman DL, Hunter LM, Holbrook M, et al. Effect of exercise on upper and lower extremity endothelial function in patients with coronary artery disease. Am J Cardiol. 2002;90(2):124–7.

    PubMed  Article  Google Scholar 

  150. Ades PA, Savage PD, Lischke S, Toth MJ, Harvey-Berino J, Bunn JY, et al. The effect of weight loss and exercise training on flow-mediated dilatation in coronary heart disease: a randomized trial. Chest. 2011;140(6):1420–7. https://doi.org/10.1378/chest.10-3289.

    PubMed  PubMed Central  Article  Google Scholar 

  151. Edwards DG, Schofield RS, Lennon SL, Pierce GL, Nichols WW, Braith RW. Effect of exercise training on endothelial function in men with coronary artery disease. Am J Cardiol. 2004;93(5):617–20. https://doi.org/10.1016/j.amjcard.2003.11.032.

    PubMed  CAS  Article  Google Scholar 

  152. Munk PS, Staal EM, Butt N, Isaksen K, Larsen AI. High-intensity interval training may reduce in-stent restenosis following percutaneous coronary intervention with stent implantation A randomized controlled trial evaluating the relationship to endothelial function and inflammation. Am Heart J. 2009;158(5):734–41. https://doi.org/10.1016/j.ahj.2009.08.021.

    PubMed  Article  Google Scholar 

  153. Kim C, Choi HE, Jung H, Kang SH, Kim JH, Byun YS. Impact of aerobic exercise training on endothelial function in acute coronary syndrome. Ann Rehabil Med. 2014;38(3):388–95. https://doi.org/10.5535/arm.2014.38.3.388.

    PubMed  PubMed Central  Article  Google Scholar 

  154. Steiner S, Niessner A, Ziegler S, Richter B, Seidinger D, Pleiner J, 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. https://doi.org/10.1016/j.atherosclerosis.2005.01.006.

    PubMed  CAS  Article  Google Scholar 

  155. Currie KD, Dubberley JB, McKelvie RS, MacDonald MJ. Low-volume, high-intensity interval training in patients with CAD. Med Sci Sports Exerc. 2013;45(8):1436–42. https://doi.org/10.1249/MSS.0b013e31828bbbd4.

    PubMed  Article  Google Scholar 

  156. Linke A, Erbs S, Hambrecht R. Exercise and the coronary circulation-alterations and adaptations in coronary artery disease. Prog Cardiovasc Dis. 2006;48(4):270–84. https://doi.org/10.1016/j.pcad.2005.10.001.

    PubMed  CAS  Article  Google Scholar 

  157. Walsh JH, Bilsborough W, Maiorana A, Best M, O’Driscoll GJ, Taylor RR, et al. Exercise training improves conduit vessel function in patients with coronary artery disease. J Appl Physiol (Bethesda, Md: 1985). 2003;95(1):20–5. https://doi.org/10.1152/japplphysiol.00012.2003.

    Article  Google Scholar 

  158. Green DJ, Walsh JH, Maiorana A, Burke V, Taylor RR, O’Driscoll JG. Comparison of resistance and conduit vessel nitric oxide-mediated vascular function in vivo: effects of exercise training. J Appl Physiol (Bethesda, Md: 1985). 2004;97(2):749–55. https://doi.org/10.1152/japplphysiol.00109.2004 (discussion 8).

    CAS  Article  Google Scholar 

  159. Hambrecht R, Wolf A, Gielen S, Linke A, Hofer J, Erbs S, et al. Effect of exercise on coronary endothelial function in patients with coronary artery disease. N Engl J Med. 2000;342(7):454–60. https://doi.org/10.1056/nejm200002173420702.

    PubMed  CAS  Article  Google Scholar 

  160. Adams V, Lenk K, Linke A, Lenz D, Erbs S, Sandri M, et al. Increase of circulating endothelial progenitor cells in patients with coronary artery disease after exercise-induced ischemia. Arterioscler Thromb Vasc Biol. 2004;24(4):684–90. https://doi.org/10.1161/01.ATV.0000124104.23702.a0.

    PubMed  CAS  Article  Google Scholar 

  161. Williams MA, Haskell WL, Ades PA, Amsterdam EA, Bittner V, Franklin BA, et al. Resistance exercise in individuals with and without cardiovascular disease: 2007 update: a scientific statement from the American Heart Association Council on Clinical Cardiology and Council on Nutrition, Physical Activity, and Metabolism. Circulation. 2007;116(5):572–84. https://doi.org/10.1161/circulationaha.107.185214.

    PubMed  Article  Google Scholar 

  162. Hambrecht R, Walther C, Mobius-Winkler S, Gielen S, Linke A, Conradi K, et al. Percutaneous coronary angioplasty compared with exercise training in patients with stable coronary artery disease: a randomized trial. Circulation. 2004;109(11):1371–8. https://doi.org/10.1161/01.cir.0000121360.31954.1f.

    PubMed  Article  Google Scholar 

  163. 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(1):107–12. https://doi.org/10.1097/HJR.0b013e3282f29aa6.

    PubMed  Article  Google Scholar 

  164. Choi HE, Lee BJ, Kim C. Impact of exercise-based cardiac rehabilitation on de novo coronary lesion in patients with drug eluting stent. Ann Rehabil Med. 2014;38(2):256–62. https://doi.org/10.5535/arm.2014.38.2.256.

    PubMed  PubMed Central  Article  Google Scholar 

  165. van Oort G, Gross DR, Spiekerman AM. Effects of eight weeks of physical conditioning on atherosclerotic plaque in swine. Am J Vet Res. 1987;48(1):51–5.

    PubMed  Google Scholar 

  166. Yang X, Li Y, Ren X, Xiong X, Wu L, Li J, et al. Effects of exercise-based cardiac rehabilitation in patients after percutaneous coronary intervention: a meta-analysis of randomized controlled trials. Sci Rep. 2017;7:44789. https://doi.org/10.1038/srep44789.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  167. Goel K, Lennon RJ, Tilbury RT, Squires RW, Thomas RJ. Impact of cardiac rehabilitation on mortality and cardiovascular events after percutaneous coronary intervention in the community. Circulation. 2011;123(21):2344–52. https://doi.org/10.1161/circulationaha.110.983536.

    PubMed  Article  Google Scholar 

  168. Altun I, Oz F, Arkaya SC, Altun I, Bilge AK, Umman B, et al. Effect of statins on endothelial function in patients with acute coronary syndrome: a prospective study using adhesion molecules and flow-mediated dilatation. J Clin Med Res. 2014;6(5):354–61. https://doi.org/10.14740/jocmr1863w.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  169. O’Driscoll G, Green D, Taylor RR. Simvastatin, an HMG-coenzyme A reductase inhibitor, improves endothelial function within 1 month. Circulation. 1997;95(5):1126–31.

    PubMed  Article  Google Scholar 

  170. Peller M, Ozieranski K, Balsam P, Grabowski M, Filipiak KJ, Opolski G. Influence of beta-blockers on endothelial function: a meta-analysis of randomized controlled trials. Cardiol J. 2015;22(6):708–16. https://doi.org/10.5603/CJ.a2015.0042.

    PubMed  Article  Google Scholar 

  171. Cheetham C, Collis J, O’Driscoll G, Stanton K, Taylor R, Green D. Losartan, an angiotensin type 1 receptor antagonist, improves endothelial function in non-insulin-dependent diabetes. J Am Coll Cardiol. 2000;36(5):1461–6.

    PubMed  CAS  Article  Google Scholar 

  172. Cheetham C, O’Driscoll G, Stanton K, Taylor R, Green D. Losartan, an angiotensin type I receptor antagonist, improves conduit vessel endothelial function in type II diabetes. Clin Sci (London, England: 1979). 2001;100(1):13–7.

    CAS  Google Scholar 

  173. O’Driscoll G, Green D, Maiorana A, Stanton K, Colreavy F, Taylor R. Improvement in endothelial function by angiotensin-converting enzyme inhibition in non-insulin-dependent diabetes mellitus. J Am Coll Cardiol. 1999;33(6):1506–11.

    PubMed  Article  Google Scholar 

  174. Collis J, Cheetham C, Dembo L, O’Driscoll J, Stanton K, Taylor R, et al. Losartan, an angiotensin type 1 receptor inhibitor, and endothelial vasodilator function in type 1 diabetes mellitus. Diab Med J Br Diab Assoc. 2000;17(7):553–4.

    CAS  Article  Google Scholar 

  175. Radenkovic M, Stojanovic M, Prostran M. Calcium channel blockers in restoration of endothelial function: systematic review and meta-analysis of randomized controlled trials. Curr Med Chem. 2018. https://doi.org/10.2174/0929867325666180713144806.

    Article  Google Scholar 

  176. Kokkinos PF, Faselis C, Myers J, Panagiotakos D, Doumas M. Interactive effects of fitness and statin treatment on mortality risk in veterans with dyslipidaemia: a cohort study. Lancet (London, England). 2013;381(9864):394–9. https://doi.org/10.1016/s0140-6736(12)61426-3.

    CAS  Article  Google Scholar 

  177. Naci H, Ioannidis JP. Comparative effectiveness of exercise and drug interventions on mortality outcomes: metaepidemiological study. Br J Sports Med. 2015;49(21):1414–22. https://doi.org/10.1136/bjsports-2015-f5577rep.

    PubMed  Article  Google Scholar 

  178. Paszkowiak JJ, Dardik A. Arterial wall shear stress: observations from the bench to the bedside. Vasc Endovasc Surg. 2003;37(1):47–57. https://doi.org/10.1177/153857440303700107.

    Article  Google Scholar 

  179. Hambrecht R, Adams V, Erbs S, Linke A, Krankel N, Shu Y, et al. Regular physical activity improves endothelial function in patients with coronary artery disease by increasing phosphorylation of endothelial nitric oxide synthase. Circulation. 2003;107(25):3152–8. https://doi.org/10.1161/01.cir.0000074229.93804.5c.

    PubMed  CAS  Article  Google Scholar 

  180. Birk GK, Dawson EA, Atkinson C, Haynes A, Cable NT, Thijssen DH, et al. Brachial artery adaptation to lower limb exercise training: role of shear stress. J Appl Physiol (Bethesda, Md: 1985). 2012;112(10):1653–8. https://doi.org/10.1152/japplphysiol.01489.2011.

    Article  Google Scholar 

  181. Tinken TM, Thijssen DH, Hopkins N, Black MA, Dawson EA, Minson CT, et al. Impact of shear rate modulation on vascular function in humans. Hypertension (Dallas, Tex: 1979). 2009;54(2):278–85. https://doi.org/10.1161/hypertensionaha.109.134361.

    CAS  Article  Google Scholar 

  182. Cesari F, Sofi F, Caporale R, Capalbo A, Marcucci R, Macchi C, et al. Relationship between exercise capacity, endothelial progenitor cells and cytochemokines in patients undergoing cardiac rehabilitation. Thromb Haemost. 2009;101(3):521–6.

    PubMed  CAS  Article  Google Scholar 

  183. Munk PS, Breland UM, Aukrust P, Ueland T, Kvaloy JT, Larsen AI. High intensity interval training reduces systemic inflammation in post-PCI patients. Eur J Cardiovasc Prev Rehabil. 2011;18(6):850–7. https://doi.org/10.1177/1741826710397600.

    PubMed  Article  Google Scholar 

  184. Haynes A, Linden MD, Robey E, Naylor LH, Ainslie PN, Cox KL, et al. Beneficial impacts of regular exercise on platelet function in sedentary older adults: evidence from a randomized 6-month walking trial. J Appl Physiol (Bethesda, Md: 1985). 2018. https://doi.org/10.1152/japplphysiol.00079.2018.

    Article  Google Scholar 

  185. de Meirelles LR, Matsuura C, Resende Ade C, Salgado AA, Pereira NR, Coscarelli PG, et al. Chronic exercise leads to antiaggregant, antioxidant and anti-inflammatory effects in heart failure patients. Eur J Prev Cardiol. 2014;21(10):1225–32. https://doi.org/10.1177/2047487313491662.

    PubMed  Article  Google Scholar 

  186. Sasaki Y, Morimoto A, Ishii I, Morita S, Tsukahara M, Yamamoto J. Preventive effect of long-term aerobic exercise on thrombus formation in rat cerebral vessels. Haemostasis. 1995;25(5):212–7.

    PubMed  CAS  Google Scholar 

  187. Lee JY, Yun SC, Ahn JM, Park DW, Kang SJ, Lee SW, et al. Impact of cardiac rehabilitation on angiographic outcomes after drug-eluting stents in patients with de novo long coronary artery lesions. Am J Cardiol. 2014;113(12):1977–85. https://doi.org/10.1016/j.amjcard.2014.03.037.

    PubMed  Article  Google Scholar 

  188. Lee HY, Kim JH, Kim BO, Byun YS, Cho S, Goh CW, et al. Regular exercise training reduces coronary restenosis after percutaneous coronary intervention in patients with acute myocardial infarction. Int J Cardiol. 2013;167(6):2617–22. https://doi.org/10.1016/j.ijcard.2012.06.122.

    PubMed  Article  Google Scholar 

  189. Gielen S, Schuler G, Hambrecht R. Exercise training in coronary artery disease and coronary vasomotion. Circulation. 2001;103(1):E1–6.

    PubMed  CAS  Article  Google Scholar 

  190. Laurent M, Daline T, Malika B, Fawzi O, Philippe V, Benoit D, et al. Training-induced increase in nitric oxide metabolites in chronic heart failure and coronary artery disease: an extra benefit of water-based exercises? Eur J Cardiovasc Prev Rehabil. 2009;16(2):215–21. https://doi.org/10.1097/HJR.0b013e3283292fcf.

    PubMed  Article  Google Scholar 

  191. Cesari F, Marcucci R, Gori AM, Burgisser C, Francini S, Sofi F, et al. Impact of a cardiac rehabilitation program and inflammatory state on endothelial progenitor cells in acute coronary syndrome patients. Int J Cardiol. 2013;167(5):1854–9. https://doi.org/10.1016/j.ijcard.2012.04.157.

    PubMed  Article  Google Scholar 

  192. Alkarmi A, Thijssen DH, Albouaini K, Cable NT, Wright DJ, Green DJ, et al. Arterial prehabilitation: can exercise induce changes in artery size and function that decrease complications of catheterization? Sports Med (Auckland, NZ). 2010;40(6):481–92. https://doi.org/10.2165/11531950-000000000-00000.

    Article  Google Scholar 

  193. Aragam KG, Dai D, Neely ML, Bhatt DL, Roe MT, Rumsfeld JS, et al. Gaps in referral to cardiac rehabilitation of patients undergoing percutaneous coronary intervention in the United States. J Am Coll Cardiol. 2015;65(19):2079–88. https://doi.org/10.1016/j.jacc.2015.02.063.

    PubMed  Article  Google Scholar 

  194. Kotseva K, Wood D, De Backer G, De Bacquer D, Pyorala K, Keil U. Cardiovascular prevention guidelines in daily practice: a comparison of EUROASPIRE I, II, and III surveys in eight European countries. Lancet (London, England). 2009;373(9667):929–40. https://doi.org/10.1016/s0140-6736(09)60330-5.

    Article  Google Scholar 

  195. de Belder MA, Ludman PF, McLenachan JM, Weston CF, Cunningham D, Lazaridis EN, et al. The national infarct angioplasty project: UK experience and subsequent developments. EuroIntervention J EuroPCR Collab Work Group Interv Cardiol Eur Soc Cardiol. 2014;10(Suppl T):T96–104. https://doi.org/10.4244/eijv10sta15.

    Article  Google Scholar 

  196. Pack QR, Squires RW, Lopez-Jimenez F, Lichtman SW, Rodriguez-Escudero JP, Lindenauer PK, et al. Participation rates, process monitoring, and quality improvement among cardiac rehabilitation programs in the United States: A NATIONAL SURVEY. J Cardiopulm Rehabil Prev. 2015;35(3):173–80. https://doi.org/10.1097/hcr.0000000000000108.

    PubMed  PubMed Central  Article  Google Scholar 

  197. Beatty AL, Bradley SM, Maynard C, McCabe JM. Referral to cardiac rehabilitation after percutaneous coronary intervention, coronary artery bypass surgery, and valve surgery: data from the clinical outcomes assessment program. Circ Cardiovasc Qual Outcomes. 2017. https://doi.org/10.1161/circoutcomes.116.003364.

    PubMed  Article  Google Scholar 

  198. Ciampricotti R, el Gamal MI. Unstable angina, myocardial infarction and sudden death after an exercise stress test. Int J Cardiol. 1989;24(2):211–8.

    PubMed  CAS  Article  Google Scholar 

  199. Goto Y, Sumida H, Ueshima K, Adachi H, Nohara R, Itoh H. Safety and implementation of exercise testing and training after coronary stenting in patients with acute myocardial infarction. Circ J. 2002;66(10):930–6.

    PubMed  Article  Google Scholar 

  200. Roffi M, Wenaweser P, Windecker S, Mehta H, Eberli FR, Seiler C, et al. Early exercise after coronary stenting is safe. J Am Coll Cardiol. 2003;42(9):1569–73.

    PubMed  Article  Google Scholar 

  201. Samuels B, Schumann J, Kiat H, Friedman J, Berman DS. Acute stent thrombosis associated with exercise testing after successful percutaneous transluminal coronary angioplasty. Am Heart J. 1995;130(5):1120–2.

    PubMed  CAS  Article  Google Scholar 

  202. Kim HS, Kim SY, Lee UJ, Kim W. Terrible stent thrombosis induced by a treadmill test performed three days after percutaneous coronary intervention. Chonnam Med J. 2014;50(1):23–6. https://doi.org/10.4068/cmj.2014.50.1.23.

    PubMed  PubMed Central  Article  Google Scholar 

  203. Nygaard TW, Beller GA, Mentzer RM, Gibson RS, Moeller CM, Burwell LR. Acute coronary occlusion with exercise testing after initially successful coronary angioplasty for acute myocardial infarction. Am J Cardiol. 1986;57(8):687–8.

    PubMed  CAS  Article  Google Scholar 

  204. Choi Y, Akazawa N, Zempo-Miyaki A, Ra SG, Shiraki H, Ajisaka R, et al. Acute effect of high-Intensity eccentric exercise on vascular endothelial function in young men. J Strength Cond Res. 2016;30(8):2279–85. https://doi.org/10.1519/jsc.0000000000000536.

    PubMed  Article  Google Scholar 

  205. Chen YW, Apostolakis S, Lip GY. Exercise-induced changes in inflammatory processes: implications for thrombogenesis in cardiovascular disease. Ann Med. 2014;46(7):439–55. https://doi.org/10.3109/07853890.2014.927713.

    PubMed  CAS  Article  Google Scholar 

  206. Atkinson CL, Carter HH, Dawson EA, Naylor LH, Thijssen DH, Green DJ. Impact of handgrip exercise intensity on brachial artery flow-mediated dilation. Eur J Appl Physiol. 2015;115(8):1705–13. https://doi.org/10.1007/s00421-015-3157-1.

    PubMed  Article  Google Scholar 

  207. Johnson BD, Mather KJ, Newcomer SC, Mickleborough TD, Wallace JP. Brachial artery flow-mediated dilation following exercise with augmented oscillatory and retrograde shear rate. Cardiovasc Ultrasound. 2012;10:34. https://doi.org/10.1186/1476-7120-10-34.

    PubMed  PubMed Central  Article  Google Scholar 

  208. Rakobowchuk M, Tanguay S, Burgomaster KA, Howarth KR, Gibala MJ, MacDonald MJ. Sprint interval and traditional endurance training induce similar improvements in peripheral arterial stiffness and flow-mediated dilation in healthy humans. Am J Physiol Regul Integr Comp Physiol. 2008;295(1):R236–42. https://doi.org/10.1152/ajpregu.00069.2008.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  209. Dawson EA, Whyte GP, Black MA, Jones H, Hopkins N, Oxborough D, et al. Changes in vascular and cardiac function after prolonged strenuous exercise in humans. J Appl Physiol (Bethesda, Md: 1985). 2008;105(5):1562–8. https://doi.org/10.1152/japplphysiol.90837.2008.

    Article  Google Scholar 

  210. Llewellyn TL, Chaffin ME, Berg KE, Meendering JR. The relationship between shear rate and flow-mediated dilation is altered by acute exercise. Acta Physiol (Oxford, England). 2012;205(3):394–402. https://doi.org/10.1111/j.1748-1716.2012.02417.x.

    CAS  Article  Google Scholar 

  211. Bond B, Hind S, Williams CA, Barker AR. The acute effect of exercise intensity on vascular function in adolescents. Med Sci Sports Exerc. 2015;47(12):2628–35. https://doi.org/10.1249/mss.0000000000000715.

    PubMed  Article  Google Scholar 

  212. Shenouda N, Skelly LE, Gibala MJ, MacDonald MJ. Brachial artery endothelial function is unchanged after acute sprint interval exercise in sedentary men and women. Exp Physiol. 2018. https://doi.org/10.1113/ep086677.

    PubMed  Article  Google Scholar 

  213. Rognmo O, Bjornstad TH, Kahrs C, Tjonna AE, Bye A, Haram PM, et al. Endothelial function in highly endurance-trained men: effects of acute exercise. J Strength Cond Res. 2008;22(2):535–42. https://doi.org/10.1519/JSC.0b013e31816354b1.

    PubMed  Article  Google Scholar 

  214. McClean C, Harris RA, Brown M, Brown JC, Davison GW. Effects of exercise intensity on postexercise endothelial function and oxidative stress. Oxid Med Cell Longev. 2015;2015:723679. https://doi.org/10.1155/2015/723679.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  215. Dawson EA, Green DJ, Cable NT, Thijssen DH. Effects of acute exercise on flow-mediated dilatation in healthy humans. J Appl Physiol (Bethesda, Md: 1985). 2013;115(11):1589–98. https://doi.org/10.1152/japplphysiol.00450.2013.

    Article  Google Scholar 

  216. Johnson BD, Padilla J, Wallace JP. The exercise dose affects oxidative stress and brachial artery flow-mediated dilation in trained men. Eur J Appl Physiol. 2012;112(1):33–42. https://doi.org/10.1007/s00421-011-1946-8.

    PubMed  CAS  Article  Google Scholar 

  217. Michaelides AP, Soulis D, Antoniades C, Antonopoulos AS, Miliou A, Ioakeimidis N, et al. Exercise duration as a determinant of vascular function and antioxidant balance in patients with coronary artery disease. Heart (Br Card Soc). 2011;97(10):832–7. https://doi.org/10.1136/hrt.2010.209080.

    CAS  Article  Google Scholar 

  218. Bailey TG, Perissiou M, Windsor M, Russell F, Golledge J, Green DJ, et al. Cardiorespiratory fitness modulates the acute flow-mediated dilation response following high-intensity but not moderate-intensity exercise in elderly men. J Appl Physiol (Bethesda, Md: 1985). 2017;122(5):1238–48. https://doi.org/10.1152/japplphysiol.00935.2016.

    Article  Google Scholar 

  219. Farsidfar F, Kasikcioglu E, Oflaz H, Kasikcioglu D, Meric M, Umman S. Effects of different intensities of acute exercise on flow-mediated dilatation in patients with coronary heart disease. Int J Cardiol. 2008;124(3):372–4. https://doi.org/10.1016/j.ijcard.2006.11.243.

    PubMed  Article  Google Scholar 

  220. 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(16):1994–2000.

    PubMed  Article  Google Scholar 

  221. Currie KD, McKelvie RS, Macdonald MJ. Flow-mediated dilation is acutely improved after high-intensity interval exercise. Med Sci Sports Exerc. 2012;44(11):2057–64. https://doi.org/10.1249/MSS.0b013e318260ff92.

    PubMed  Article  Google Scholar 

  222. Currie KD, McKelvie RS, Macdonald MJ. Brachial artery endothelial responses during early recovery from an exercise bout in patients with coronary artery disease. Biomed Res Int. 2014;2014:591918. https://doi.org/10.1155/2014/591918.

    PubMed  PubMed Central  Article  Google Scholar 

  223. McLenachan JM, Williams JK, Fish RD, Ganz P, Selwyn AP. Loss of flow-mediated endothelium-dependent dilation occurs early in the development of atherosclerosis. Circulation. 1991;84(3):1273–8.

    PubMed  CAS  Article  Google Scholar 

  224. Gordon JB, Ganz P, Nabel EG, Fish RD, Zebede J, Mudge GH, et al. Atherosclerosis influences the vasomotor response of epicardial coronary arteries to exercise. J Clin Investig. 1989;83(6):1946–52. https://doi.org/10.1172/jci114103.

    PubMed  CAS  Article  PubMed Central  Google Scholar 

  225. Boos CJ, Balakrishnan B, Lip GY. The effects of exercise stress testing on soluble E-selectin, von Willebrand factor, and circulating endothelial cells as indices of endothelial damage/dysfunction. Ann Med. 2008;40(1):66–73. https://doi.org/10.1080/07853890701652833.

    PubMed  CAS  Article  Google Scholar 

  226. Hays AG, Stuber M, Hirsch GA, Yu J, Schar M, Weiss RG, et al. Non-invasive detection of coronary endothelial response to sequential handgrip exercise in coronary artery disease patients and healthy adults. PLoS One. 2013;8(3):e58047. https://doi.org/10.1371/journal.pone.0058047.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  227. Hays AG, Iantorno M, Soleimanifard S, Steinberg A, Schar M, Gerstenblith G, et al. Coronary vasomotor responses to isometric handgrip exercise are primarily mediated by nitric oxide: a noninvasive MRI test of coronary endothelial function. Am J Physiol Heart Circ Physiol. 2015;308(11):H1343–50. https://doi.org/10.1152/ajpheart.00023.2015.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  228. Togni M, Windecker S, Cocchia R, Wenaweser P, Cook S, Billinger M, et al. Sirolimus-eluting stents associated with paradoxic coronary vasoconstriction. J Am Coll Cardiol. 2005;46(2):231–6. https://doi.org/10.1016/j.jacc.2005.01.062.

    PubMed  CAS  Article  Google Scholar 

  229. Puricel S, Kallinikou Z, Espinola J, Arroyo D, Goy JJ, Stauffer JC, et al. Comparison of endothelium-dependent and -independent vasomotor response after abluminal biodegradable polymer biolimus-eluting stent and persistent polymer everolimus-eluting stent implantation (COMPARE-IT). Int J Cardiol. 2016;202:525–31. https://doi.org/10.1016/j.ijcard.2015.09.085.

    PubMed  Article  Google Scholar 

  230. Rummens JL, Daniels A, Dendale P, Hensen K, Hendrikx M, Berger J, et al. Suppressed increase in blood endothelial progenitor cell content as result of single exhaustive exercise bout in male revascularised coronary artery disease patients. Acta Clin Belg. 2012;67(4):262–9. https://doi.org/10.2143/acb.67.4.2062670.

    PubMed  CAS  Article  Google Scholar 

  231. Kazmierski M, Wojakowski W, Michalewska-Wludarczyk A, Podolecka E, Kotowski M, Machalinski B, et al. Exercise-induced mobilisation of endothelial progenitor cells in patients with premature coronary heart disease. Kardiologia polska. 2015;73(6):411–8. https://doi.org/10.5603/KP.a2014.0248.

    PubMed  Article  Google Scholar 

  232. 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(6):2877–85.

    PubMed  CAS  Article  Google Scholar 

  233. Ikarugi H, Shibata M, Shibata S, Ishii H, Taka T, Yamamoto J. High intensity exercise enhances platelet reactivity to shear stress and coagulation during and after exercise. Pathophysiol Haemost Thromb. 2003;33(3):127–33.

    PubMed  Article  Google Scholar 

  234. Ikarugi H, Yamamoto J. The exercise paradox may be solved by measuring the overall thrombotic state using native blood. Drug Discov Ther. 2017;11(1):15–9. https://doi.org/10.5582/ddt.2016.01077.

    PubMed  Article  Google Scholar 

  235. Posthuma JJ, van der Meijden PE, Ten Cate H, Spronk HM. Short- and Long-term exercise induced alterations in haemostasis: a review of the literature. Blood Rev. 2015;29(3):171–8. https://doi.org/10.1016/j.blre.2014.10.005.

    PubMed  Article  Google Scholar 

  236. Cadroy Y, Pillard F, Sakariassen KS, Thalamas C, Boneu B, Riviere D. Strenuous but not moderate exercise increases the thrombotic tendency in healthy sedentary male volunteers. J Appl Physiol (Bethesda, Md: 1985). 2002;93(3):829–33. https://doi.org/10.1152/japplphysiol.00206.2002.

    Article  Google Scholar 

  237. 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(2):293–301. https://doi.org/10.1160/th09-09-0633.

    PubMed  CAS  Article  Google Scholar 

  238. 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. https://doi.org/10.1186/1471-2261-8-11.

    PubMed  PubMed Central  Article  Google Scholar 

  239. Li N, Wallen NH, Hjemdahl P. Evidence for prothrombotic effects of exercise and limited protection by aspirin. Circulation. 1999;100(13):1374–9.

    PubMed  CAS  Article  Google Scholar 

  240. 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. Kardiologia polska. 2006;64(10):1094–100 (discussion 101).

    PubMed  Google Scholar 

  241. Tokuue J, Hayashi J, Hata Y, Nakahara K, Ikeda Y. Enhanced platelet aggregability under high shear stress after treadmill exercise in patients with effort angina. Thromb Haemost. 1996;75(5):833–7.

    PubMed  CAS  Article  Google Scholar 

  242. Wang JS, Liao CH. Moderate-intensity exercise suppresses platelet activation and polymorphonuclear leukocyte interaction with surface-adherent platelets under shear flow in men. Thromb Haemost. 2004;91(3):587–94. https://doi.org/10.1160/th03-10-0644.

    PubMed  CAS  Article  Google Scholar 

  243. Levine GN, Bates ER, Bittl JA, Brindis RG, Fihn SD, Fleisher LA, et al. 2016 ACC/AHA guideline focused update on duration of dual antiplatelet therapy in patients with coronary artery disease: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. J Thorac Cardiovasc Surg. 2016;152(5):1243–75. https://doi.org/10.1016/j.jtcvs.2016.07.044.

    PubMed  Article  Google Scholar 

  244. Mehta SR, Yusuf S, Peters RJ, Bertrand ME, Lewis BS, Natarajan MK, et al. Effects of pretreatment with clopidogrel and aspirin followed by long-term therapy in patients undergoing percutaneous coronary intervention: the PCI-CURE study. Lancet (London, England). 2001;358(9281):527–33.

    CAS  Article  Google Scholar 

  245. 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(6):767–73. https://doi.org/10.1016/j.amjcard.2007.11.006.

    PubMed  Article  Google Scholar 

  246. 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(1):77–84. https://doi.org/10.1007/s00392-010-0215-x.

    PubMed  CAS  Article  Google Scholar 

  247. Lominadze D, Dean WL, Tyagi SC, Roberts AM. Mechanisms of fibrinogen-induced microvascular dysfunction during cardiovascular disease. Acta Physiol (Oxford, England). 2010;198(1):1–13. https://doi.org/10.1111/j.1748-1716.2009.02037.x.

    CAS  Article  Google Scholar 

  248. Haynes A, Linden MD, Robey E, Naylor LH, Cox KL, Lautenschlager NT, et al. Relationship between monocyte-platelet aggregation and endothelial function in middle-aged and elderly adults. Physiol Rep. 2017. https://doi.org/10.14814/phy2.13189.

    PubMed  PubMed Central  Article  Google Scholar 

  249. 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(3):301–7.

    PubMed  CAS  Article  Google Scholar 

  250. Tozzi-Ciancarelli MG, Penco M, Di Massimo C. Influence of acute exercise on human platelet responsiveness: possible involvement of exercise-induced oxidative stress. Eur J Appl Physiol. 2002;86(3):266–72.

    PubMed  CAS  Article  Google Scholar 

  251. Silvestro A, Scopacasa F, Oliva G, de Cristofaro T, Iuliano L, Brevetti G. Vitamin C prevents endothelial dysfunction induced by acute exercise in patients with intermittent claudication. Atherosclerosis. 2002;165(2):277–83.

    PubMed  CAS  Article  Google Scholar 

  252. Onogi F, Saitoh S, Aikawa K, Ishibashi T, Maruyama Y. Antioxidant is a useful supportive agent for the treatment of coronary vasospasm with endothelial dysfunction in pig. Coron Artery Dis. 2007;18(2):133–40. https://doi.org/10.1097/MCA.0b013e328010a48b.

    PubMed  Article  Google Scholar 

  253. Aikawa K, Saitoh S, Muto M, Osugi T, Matsumoto K, Onogi F, et al. Effects of antioxidants on coronary microvascular spasm induced by epicardial coronary artery endothelial injury in pigs. Coron Artery Dis. 2004;15(1):21–30.

    PubMed  Article  Google Scholar 

  254. Lyamina NP, Razborov IB, Karpov ES. Clinical and economic aspects of meldonium as part of physical rehabilitation programs in patients with coronary heart disease after percutaneous coronary interventions. Kardiologiia. 2016;56(8):13–8.

    PubMed  CAS  Article  Google Scholar 

  255. Cook CM, Ahmad Y, Howard JP, Shun-Shin MJ, Sethi A, Clesham GJ, et al. Impact of percutaneous revascularization on exercise hemodynamics in patients with stable coronary disease. J Am Coll Cardiol. 2018;72(9):970–83. https://doi.org/10.1016/j.jacc.2018.06.033.

    PubMed  PubMed Central  Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Research Institute for Sport and Exercise Science, Liverpool John Moores University, Liverpool, L3 3AF, UK

    Andrea Tryfonos & Ellen A. Dawson

  2. School of Human Sciences (Exercise and Sport Science), The University of Western Australia, Crawley, WA, 6009, Australia

    Daniel J. Green

Authors
  1. Andrea Tryfonos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel J. Green
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ellen A. Dawson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ellen A. Dawson.

Ethics declarations

Conflict of interest

Andrea Tryfonos, Daniel J. Green and Ellen A. Dawson declare that they have no conflicts of interest.

Funding

Prof. Green is funded by the National Health and Medical Research Council of Australia Principal Research Fellowship (1080914).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tryfonos, A., Green, D.J. & Dawson, E.A. Effects of Catheterization on Artery Function and Health: When Should Patients Start Exercising Following Their Coronary Intervention?. Sports Med 49, 397–416 (2019). https://doi.org/10.1007/s40279-019-01055-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40279-019-01055-3