Skip to main content
SpringerLink
Log in

Effects of Preconditioning on Coronary Perfusion in Cardiac Ischemia and Reperfusion

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

Recent studies have demonstrated that ischemic preconditioning prevents reperfusion-induced endothelial dysfunction. However, the question of the influence of preconditioning on the occurrence of the no-reflow phenomenon remains open. The receptor mechanisms of the cardioprotective and vasoprotective effects of preconditioning are different. The ability of preconditioning to prevent reperfusion-induced endothelial dysfunction is associated with activation of bradykinin B2 receptors and is independent of stimulation of adenosine receptors. The vasoprotective effect of preconditioning is mediated by mechanisms associated with activation of protein kinase C, NO synthase, and cyclooxygenase, the opening of mitochondrial KATP channels, and increases in the antioxidant defense of the heart. Delayed preconditioning also has an endothelium-protecting effect. Triggers for these effects are NO•, O2 •, and peroxynitrite, and endothelial NO synthase may be the end effector is.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. N. A. Zenkov, V. Z. Lankin, and E. B. Men’shchikova, Oxidative Stress: Biochemical and Pathophysiological Aspects [in Russian], MAIK Nauka/Interperiodika, Moscow (2001).

    Google Scholar 

  2. V. A. Kazakov, I. V. Sukhodolo,V. M. Shipulin, and O. N. Ogurkova, “The search for molecular markers of post-operative remodeling of the left ventricle in patients with ischemic cardiomyopathy,” Sib. Med. Zh. (Tomsk), 25, No. 2, 34–37 (2010).

    Google Scholar 

  3. P. F. Litvitskii, V. A. Sandrikov, and E. A. Demurov, Adaptive and Pathogenic Effects of Reperfusion and Reoxygenation of the Myocardium [in Russian], Meditsina, Moscow (1994).

    Google Scholar 

  4. L. N. Maslov, Yu. B. Lishmanov, and N. V. Solenkova, “Adaptation of the myocardium to ischemia. The first phase of ischemic preconditioning,” Usp. Fiziol. Nauk., 37, No. 3, 25–41 (2006).

    PubMed  CAS  Google Scholar 

  5. L. N. Maslov, “New approaches to the prophylaxis and treatment of ischemic and reperfusion damage to the heart in acute myocardial infarction,” Sib. Med. Zh. (Tomsk), 25, No. 2, 17–24 (2010).

    Google Scholar 

  6. V. M. Shipulin, B. N. Kozlov, A. V. Evtushenko, and Yu. Yu. Vecherskii, “Contemporary strategies in the treatment of cardiac failure and heart surgery,” Sib. Med. Zh. (Tomsk), 25, No. 2, 4–12 (2010).

    Google Scholar 

  7. E. Andelova, M. Bartekova, D. Pancza, et. al., “The role of NO in ischemia/reperfusion injury in isolated rat heart,” Gen. Physiol. Biophys., 24, No. 4, 411–426 (2005).

    PubMed  CAS  Google Scholar 

  8. L. Argaud, G. Rioufol. M. Lièvre, et. al., “Preconditioning during coronary angioplasty: no influence of collateral perfusion or the size of the area at risk,” Eur. Heart. J., 25, No. 22, 2019–2025 (2004).

    Article  PubMed  Google Scholar 

  9. B. Bauer, B. Z. Simkhovich, R. A. Kloner, and K. Przyklenk “Does preconditioning protect the coronary vasculature from subsequent ischemia/reperfusion injury?” Circulation, 88, No. 2, 659–672 (1993).

    Article  PubMed  CAS  Google Scholar 

  10. J. F. Bouchard, J. Chouinard, and D. Lamontagne, “Role of kinins in the endothelial protective effect of ischaemic preconditioning,” Br. J. Pharmacol., 123, No. 3, 413–420 (1998).

    Article  PubMed  CAS  Google Scholar 

  11. J. F. Bouchard, J. Chouinard, and D. Lamontagne, “Participation of prostaglandin E2 in the endothelial protective effect of ischaemic preconditioning in isolated rat heart,” Cardiovasc. Res., 45, No. 2, 418–427 (2000).

    Article  PubMed  CAS  Google Scholar 

  12. B. L. Fubkin, S. T. Shearer, J. Vinten-Johansen, et. al., “Preconditioning during simulated MIDCABG attenuates blood flow defects and neutrophil accumulation,” Ann. Thorac, Surg., 66, No. 3, 726–732 (1998).

    Article  Google Scholar 

  13. M. J. Butler, W. Chan, A. J. Taylor, et. al., “Management of the noreflow phenomenon,” Pharmacol. Ther., 132, No. 1, 72–85 (2011).

    Article  PubMed  CAS  Google Scholar 

  14. S. Chlopicki, M. Lomnicka, and R. H. Gryglewski, “Reversal of the postischaemic suppression of coronary function in perfused guinea pig heart by ischaemic preconditioning,” J. Physiol. Pharmacol., 50, No. 4, 605–615 (1999).

    PubMed  CAS  Google Scholar 

  15. J. C. Cutrn, M. G. Perrelli, B. Cavalieri, et. al., “Microvascular dysfunction induced by reperfusion injury and protective effect of ischemic preconditioning,” Free Radic. Biol. Med., 33, No. 9, 1200–1208 (2002).

    Article  PubMed  Google Scholar 

  16. I. M. Dauber, K. M. VanBenthuysen, I. F. McMurtry, et. al., “Functional coronary microvascular injury evidence as increased permeability of the brief ischemia and reperfusion,” Circ. Res., 66, No. 4, 986–998 (1990).

    Article  PubMed  CAS  Google Scholar 

  17. I. M. Dauber, E. J. Lesnefsky, K. M. VanBenthuysen, et. al., “Reactive oxygen metabolite scavengers decrease functional coronary microvascular injury due to ischemia-reperfusion,” Am. J. Physiol., 260, No. 1, H42–H49 (1991).

    PubMed  CAS  Google Scholar 

  18. T. Dost, M. V. Cohen, and J. M. Downey, “Redox signalling triggers protection during the reperfusion rather than the ischemic phase of preconditioning,” Basic Res. Cardiol., 103, No. 4, 378–384 (2008).

    Article  PubMed  Google Scholar 

  19. M. Duda, E. Czarnowska, M. Kurzelewski, et. al., “Ischemic preconditioning prevents endothelial dysfunction, P-selectin expression, and neutrophil adhesion by preventing endothelial and O2 − generation in the post-ischemia guinea-pig heart,” J. Physiol. Pharmacol., 57, No. 4, 553–569 (2006).

    PubMed  CAS  Google Scholar 

  20. M. Duda, A. Konior, E. Klemenska, and A. Beresewicz, “Preconditioning protects endothelium by preventing ET-1-induced activation of NADPH oxidase and xanthine oxidase in post-ischemic heart,” J. Mol. Cell. Cardiol., 42, No. 2, 400–410 (2007).

    Article  PubMed  CAS  Google Scholar 

  21. J. Feng, C. Bianchi, and F. W. Sellke, “Bradykinin preconditioning preserves coronary microvascular reactivity during cardioplegiareperfusion,” Ann. Thorac. Surg., 79, No. 3, 911–916 (2005).

    Article  PubMed  Google Scholar 

  22. S. Funaro, L. Galiuto, F. Boccalini, et. al., “Determinants of microvascular damage recovery after acute myocardial infarction: results from the acute myocardial infarction contrast imaging (AMICI) multi-centre study,” Eur. J. Echocardiogr., 12, No. 4, 306–312 (2011).

    Article  PubMed  Google Scholar 

  23. G. J. Gross, S. T. O’Rourke, L. R. Pelc, and D. C. Warltier, “Myocardial and endothelial dysfunction after multiple, brief coronary occlusions: role of oxygen radials,” Am. J. Physiol., 263, No. 6, H1703–H1709 (1992).

    PubMed  CAS  Google Scholar 

  24. S. L. Hale and R. A. Kloner, “Ischemic preconditioning and myocardial hypothermia in rabbits with prolonged coronary artery occlusion,” Am. J. Physiol., 276, No. 6, H2029–H2034 (1999).

    PubMed  CAS  Google Scholar 

  25. T. Hirai, M. Fujita, N. Yoshida, et. al., “Importance of ischemic preconditioning and collateral circulation for left ventricular functional recovery in patients with successful intracoronary thrombolysis for acute myocardial infarction,” Am. Heart J., 126, No. 4, 827–831 (1993).

    Article  PubMed  CAS  Google Scholar 

  26. L. D. Horwitz, D. Kaufman, M. W. Keller, and Y. Kong, “Time course of coronary endothelial healing after injury due to ischemia and reperfusion,” Circulation, 90, No. 5, 2439–2447 (1994).

    Article  PubMed  CAS  Google Scholar 

  27. N. Kaeffer, V. Richard, and C. Thuillez, “Delayed coronary endothelial protection 24 hours after preconditioning: role of free radicals,” Circulation, 96, No. 7, 2311–2316 (1997).

    Article  PubMed  CAS  Google Scholar 

  28. S. J. Kapadia, J. S. Terlato, and A. S. Most, “Presence of a critical coronary artery stenosis does not abolish the protective effect of ischemic preconditioning,” Circulation, 95, No. 5, 1286–1292 (1997).

    Article  PubMed  CAS  Google Scholar 

  29. L. J. Kaplan, C. F. Bellows, H. Blum, et. al., “Ischemic preconditioning preserves end-ischemic ATP, enhancing functional recovery and coronary flow during reperfusion,” J. Surg. Res., 57, No. 1, 179–184 (1994).

    Article  PubMed  CAS  Google Scholar 

  30. M. Kawasuji, M. Ikeda, N. Sakakibara, et. al., “Near-infrared monitoring of myocardial oxygenation during ischemic preconditioning,” Ann. Thorac. Surg., 69, No. 6, 1806–1810 (2000).

    Article  PubMed  CAS  Google Scholar 

  31. Y. D. Kim, J. S. Fomsgaard, K. F. Heim, et. al., “Brief ischemia-reperfusion induces stunning of endothelium in canine coronary artery,” Circulation, 85, No. 4, 1473–1482 (1992).

    Article  PubMed  CAS  Google Scholar 

  32. R. A. Kloner, C. E. Ganote, and R. B. Jennings, “The ‘no-reflow’ phenomenon after temporary coronary occlusion in the dog,” J. Clin. Invest., 54, No. 6, 1496–1508 (1974).

    Article  PubMed  CAS  Google Scholar 

  33. R. A. Kloner, R. E. Rude, N. Carlson, et. al., “Ultrastructural evidence of microvascular damage and myocardial cell injury after coronary artery occlusion: which comes first?” Circulation, 62, No. 5, 945–952 (1980).

    Article  PubMed  CAS  Google Scholar 

  34. R. A. Kloner and K. J. Alker, “The effect of streptokinase on intramyocardial hemorrhage, infarct size, and the no-reflow phenomenon during coronary reperfusion,” Circulation, 70, No. 3, 513–521 (1984).

    Article  PubMed  CAS  Google Scholar 

  35. M. Kurzelewski, E. Czarnowska, M. Maczewski, and A. Beresewicz, “Effect of ischemic preconditioning on endothelial dysfunction and granulocyte adhesion in isolated guinea-pig hearts subjected to ischemia-reperfusion,” J. Physiol. Pharmacol., 50, No. 4, 617–628 (1999).

    PubMed  CAS  Google Scholar 

  36. K. Laude, V. Richard, J. P. Henry, et. al., “Evidence against a role of inducible nitric oxide synthase neuron the endothelial protective effects of delayed preconditioning,” Br. J. Pharmacol., 130, No. 7, 1547–1552 (2000).

    Article  PubMed  CAS  Google Scholar 

  37. K. Laude, C. Tuillez, and V. Richard, “Peroxynitrite triggers a delayed resistance of coronary endothelial cells against ischemia-reperfusion injury,” Am. J. Heart Circ. Physiol., 283, No. 4, H1418–H1423 (2002).

    CAS  Google Scholar 

  38. K. Laude, P. Beauchamp, C. Thuillez, and V. Richard, “Endothelial protective effects of preconditioning,” Cardiovasc. Res., 55, No. 3, 466–473 (2002).

    Article  PubMed  CAS  Google Scholar 

  39. K. Laude, J. Favre, C. Thuillez, and V. Richard, “NO produced by endothelial NO synthase is a mediator of delayed preconditioning-induced endothelial protection,” Am. J. Physiol. Heart Circ. Physiol., 284, No. 6, H2053–H2060 (2003).

    PubMed  CAS  Google Scholar 

  40. K. E. Loke and O. L. Woodman, “Preconditioning improves myocardial functional and reflow, but not vascular reactivity, after ischaemia and reperfusion in anaesthetized dogs,” Clin. Exp. Pharmacol. Physiol., 25, No. 7–8, 552–558 (1998).

    Article  PubMed  CAS  Google Scholar 

  41. M. Maczewsk and A. Beresewicz, “The role of adenosine and ATP-sensitive potassium channels in the protection afforded by ischemic preconditioning against the post-ischemic endothelial dysfunction in guinea-pig hearts,” J. Mol. Cell. Cardiol., 30, No. 9, 1735–1747 (1998).

    Article  Google Scholar 

  42. M. Maczewski, M. Duda, W. Pawlak, and A. Beresewicz, “Endothelial protection from reperfusion injury by ischemic preconditioning and diazoxide involves a SOD-like anti-O2 − mechanism,” Physiol. Pharmacol., 55, No. 3, 537–550 (2004).

    CAS  Google Scholar 

  43. J. L. Mehta, W. W. Nichols, W. H. Donnelly, et. al., “Impaired canine coronary vasodilator response to acetylcholine and bradykinin after occlusion -reperfusion,” Circulation, 88, No. 1, 223–234 (1993).

    Article  Google Scholar 

  44. M. Miyamae, H. Fujiwara, M. Ikda, et. al., “Preconditioning improves energy metabolism during reperfusion but does not attenuate myocardial stunning in porcine hearts,” Circulation, 88, No. 1, 223–234 (1993).

    Article  PubMed  CAS  Google Scholar 

  45. U. M. Mortensen, B. L. Norgaard, J. E. Nielsen-Kudski, et. al., “A phase of increased ST elevation during coronary occlusion following ischemic preconditioning,” Basic Res. Cardiol., 101, No. 2, 140–148 (2006).

    Article  PubMed  Google Scholar 

  46. C. A. Murry, R. B. Jennings, and K. A. Reimer, “Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium,” Circulation, 74, No. 5, 1124–1136 (1986).

    Article  PubMed  CAS  Google Scholar 

  47. C. E. Murry, V. J. Richard, R. B. Jennings, and K. A. Reimer, “Myocardial protection is lost before contractile function recovers from ischemic preconditioning,” Am. J. Physiol., 260, No. 3, H796–H804 (1991).

    PubMed  CAS  Google Scholar 

  48. B. Ostadol and F. Kolar, Cardiac Ischemia: From Injury to Protection, Kluwer Academic Press, Boston, Dordrecht, London (1999).

    Book  Google Scholar 

  49. P. Ouyang, L. C. Becker, M. B. Effron, et. al., “Hemodynamic vascular forces contribute to impaired endothelium-dependent vasodilation in reperfused canine epicardial coronary arteries,” J. Am. Coll. Cardiol., 23, No. 5, 1216–1223 (1994).

    Article  PubMed  CAS  Google Scholar 

  50. T. Reffelmann and R. A. Kloner, “Is microvascular protection by cariporide and ischemia preconditioning causally linked to myocardial salvage?” Am. J. Physiol. Heart Circ. Physiol., 284, No. 4, H1134–H1141 (2003).

    PubMed  CAS  Google Scholar 

  51. T. Reffelmann and R. A. Kloner, “The no-reflow phenomenon: A basic mechanism of myocardial ischemia and reperfusion,” Basic Res. Cardiol., 101, No. 5, 359–372 (2006).

    Article  PubMed  Google Scholar 

  52. K. A. Reimer, C. E. Murry, I. Yamasawa, et. al., “Four brief periods of myocardial ischemia cause no cumulative ATP loss or necrosis,” Am. J. Physiol., 251, No. 6, Part 2, H1306–H1315 (1986).

    Google Scholar 

  53. U. S. Ryan and R. E. Worthington, “Cell-cell contact mechanisms,” Curr. Opin. Immunol., 4, No. 1, 33–37 (1992).

    Article  PubMed  CAS  Google Scholar 

  54. T. Saito, E. Fushimi, T. Abe, et. al., “Augmented contractile response to endothelin and blunted endothelium-dependent relaxation in postischemic reperfused arteries,” Jpn. Circ. J., 56, No. 7, 657–670 (1992).

    Article  PubMed  CAS  Google Scholar 

  55. W. K. Summers and R. L. Jamison, “The no-reflow phenomenon in renal ischemia,” Lab. Invest., 25, No. 6, 635–643 (1971).

    PubMed  CAS  Google Scholar 

  56. S. Takeshima, J. Vaage, and G. Valen, “Preconditioning the globally ischaemic, isolated rat heart: the impact of the preconditioning model on post-ischaemic systolic and diastolic function,” Scand. J. Clin. Lab. Invest., 57, No. 7, 637–646 (1997).

    Article  PubMed  CAS  Google Scholar 

  57. V. H. Thourani, M. Nakamura, I. G. Duarte, et. al., “Ischemic preconditioning attenuates postischemic coronary artery endothelial dysfunction in a model of minimally invasive direct coronary artery bypass grafting,” J. Thorac. Cardiovasc. Surg., 117, No. 2, 383–389 (1999).

    Article  PubMed  CAS  Google Scholar 

  58. M. Tofukuji, C. Metais, J. Li, et. al., “Effects of ischemic preconditioning on myocardial perfusion, function, and microvascular regulation,” Circulation, 98, No. 19, Supplement, II197–II204 (1998).

  59. P. S. Tsao, N. Aoki, D. J. Lefer, et. al., “Time course of endothelial dysfunction and myocardial injury during myocardial ischemia and reperfusion in the cat,” Circulation, 82, No. 4, 1402–1412 (1990).

    Article  PubMed  CAS  Google Scholar 

  60. K. A. VanBenthuysen, I. F. McMurtry, and L. D. Horwitz, “Reperfusion after acute coronary occlusion in dogs impairs endothelium-dependent relaxation to acetylcholine and augments contractile activity in vitro,” J. Clin. Invest., 79, No. 1, 265–274 (1987).

    Article  PubMed  CAS  Google Scholar 

  61. N. Vladic, Z. D. Ge, T. Leucker, et. al., “Decreased tetrahydrobiopterin and disrupted association of Hsp90 with eNOS by hyper-glycemia impair myocardial ischemic preconditioning,” Am. J. Physiol. Heart Circ. Physiol., 301, No. 5, H2130–H2139 (2011).

    Article  PubMed  CAS  Google Scholar 

  62. X. Wu, G. S. Mintz, A. J. Lansky, et. al., “The relationship between attenuated plaque identified by intravascular ultrasound and no-reflow after stenting in acute myocardial infarction: the HORIZONS-AMI (Harmonizing Outcomes with Revascularization and Stents in Acute Myocardial Infarction) trial,” JACC Cardiovasc. Interv., 4, No. 5, 495–502 (2011).

    Article  PubMed  Google Scholar 

  63. H. Yamagishi, K. Akioka, K. Hirata, et. al., “Effects of preinfarction angina on myocardial injury in patients with acute myocardial infarction: a study with resting 123I-BMIPP and 201Tl myocardial SPECT,” J. Nucl. Med., 41, No. 5, 830–836 (2000).

    PubMed  CAS  Google Scholar 

  64. D. M. Yellon and J. M. Downey, “Preconditioning the myocardium: from cellular physiological to clinical cardiology,” Physiol. Rev., 83, No. 4, 1113–1151 (2003).

    PubMed  CAS  Google Scholar 

  65. J. L. Zhao, Y. J. Yang, S. J. You, et. al., “Beneficial effects of ischemic preconditioning on myocardial no-reflow in a mini-swine model of acute myocardial infarction and reperfusion,” Acta Acad. Med. Sin., 27, No. 4, 486-490 (2005).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Research Institute of Cardiology, Siberian Branch, Russian Academy of Medical Sciences, 111 Kievskaya Street, 634012, Tomsk, Russia

    L. N. Maslov, Yu. B. Lishmanov, A. V. Krylatov & E. I. Barzakh

  2. Department of Pathology, University of Kentucky, Lexington, Kentucky, USA

    P. Oeltgen

  3. Department of Physiology, Fourth Military Medical University, Xian, Shaanxi Province, China

    Jian-Ming Pei

  4. A. A. Bogomolets Institute of Physiology, Ukrainian National Academy of Science, Kiev, Ukraine

    A. G. Portnichenko

  5. Department of Medical Chemistry and Natural Products, Hebrew University of Jerusalem, Jerusalem, Israel

    R. Mechoulam

Authors
  1. L. N. Maslov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu. B. Lishmanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. Oeltgen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jian-Ming Pei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. V. Krylatov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. E. I. Barzakh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. G. Portnichenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. R. Mechoulam
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. N. Maslov.

Additional information

Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 98, No. 4, pp. 433–448, April, 2012.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maslov, L.N., Lishmanov, Y.B., Oeltgen, P. et al. Effects of Preconditioning on Coronary Perfusion in Cardiac Ischemia and Reperfusion. Neurosci Behav Physi 43, 1039–1048 (2013). https://doi.org/10.1007/s11055-013-9848-3

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-013-9848-3

Keywords

Search

Navigation