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The Phenomenon of Remote Preconditioning of the Heart and Its Main Manifestations

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Remote ischemic preconditioning prevents reperfusion apoptosis of cardiomyocytes and has infarct-limiting effects which persist in experiments on isolated perfused hearts. Remote preconditioning promotes recovery of cardiac contractility during reperfusion but has no effect on the frequency of occlusional and reperfusional ventricular arrhythmias. Remote preconditioning has a moderate anti-inflammatory effect. This article provides a review and the conclusions are based on published data.

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References

  1. E. A. Bautin, M. M. Galagudza, S. V. Datsenko, et al., “Effects of remote ischemic preconditioning on the course of the post-operative period in isolated prosthetization of the aortic valve,” Anesteziol. Reanimatol., No. 3, 11–17 (2014).

  2. A. N. Bogomolov, K. L. Kozlov, and O. N. Kurochkina, “Survival of elderly people after coronary stenting in acute myocardial infarction over eight years of observation: a retrospective analysis,” Usp. Gerontol., 25, No. 3, 468–473 (2012).

    CAS  Google Scholar 

  3. M. M. Galagudza, “Effects of local and remote preconditioning of the myocardium on the incidence and severity of experimentally induced ischemic tachyarrhythmia,” Vestn. Ros. Akad. Med. Nauk., No. 4, 12–17 (2007).

  4. N. V. Naryzhnaya and L. N. Maslov, “Ischemic and reperfusional heart damage: main signs and molecular mechanism,” Byull. Fed. Tsen. Serd. Krov. Endokrinol., No. 5, 56–67 (2012).

  5. N. N. Petrishchev, E. V. Shlyakto, V. A. Tsyrlin, et al., “The role of oxygen free radicals in the mechanisms of local and remote ischemic preconditioning of the myocardium,” Vestn. Ros. Akad. Med. Nauk., No. 8, 10–15 (2006).

  6. A. G. Syrkina, N. V. Belokopytova, V. A. Markov, and A. D. Erlikh, “How national and clinical guidelines for the treatment of acute coronary syndrome with ST segment elevation are implemented in in a moderately urbanized Siberian city, based on data from the REKORD2 register,” Sib. Med. Zh., 28, No. 3, 19–23 (2013).

    Google Scholar 

  7. E. V. Shlyakhto, E. M. Nifontov, and M. M. Galagudza, “Pre- and postconditioning as means of cardioprotection,: pathophysiological and clinical aspects,” Zh. Serdech. Nedostat., 9, No. 1, 4–10 (2008).

    Google Scholar 

  8. L. A. Ahmed, H. A. Salem, A. S. Attia, and A. M. Agha, “Comparative study of the cardioprotective effects of local and remote preconditioning in ischemia/reperfusion injury,” Life Sci., 90, No. 7–8, 249–256 (2012).

    Article  CAS  PubMed  Google Scholar 

  9. M. Albrecht, K. Zitta, B. Bein, et al., “Remote ischemic preconditioning regulates HIF-la levels, apoptosis and inflammation in heart tissue of cardiosurgical patients: a pilot experimental study,” Basic Res. Cardiol., 108, No. 1, 314 (2013).

    Article  PubMed  Google Scholar 

  10. Y. Birnbaum, S. L. Hale, and R. A. Kloner, “Ischemic preconditioning at a distance: reduction of myocardial infarct size by partial reduction of blood supply combined with rapid stimulation of the gastrocnemius muscle in the rabbit,” Circulation, 96, No. 5, 1641–1646 (1997).

    Article  CAS  PubMed  Google Scholar 

  11. R. A. Byrne, G. Ndrepepa, S. Braun, et al., “Peak cardiac troponin-T level, scintigraphic myocardial infarct size and one-year prognosis in patients undergoing primary percutaneous coronary intervention for acute myocardial infarction,” Am. J. Cardiol., 106, No. 9, 1212–1217 (2010).

    Article  CAS  PubMed  Google Scholar 

  12. J. Buber, A. Laish-Farkash, N. Koren-Morag, et al., “Cardiac troponin elevation pattern in patients undergoing a primary percutaneous coronary intervention for ST-segment elevation myocardial infarction: characterization and relationship with cardiovascular events during hospitalization,” Coron. Artery Dis., 26, No. 6, 503–509 (2015).

    Article  PubMed  Google Scholar 

  13. Z. P. Cai, N. Parajuli, X. Zheng, and L. Becker, “Remote ischemic preconditioning confers late protection against myocardial ischemia-reperfusion injury in mice by upregulating interleukin-10,” Basic Res. Cardiol., 107, No. 4, 277, No. 2012.

  14. X. G. Chen, B. Y. Wu, J. K. Wang, and T. Bai, “Mechanism of the protective effects of noninvasive limbs preconditioning on myocardial ischemia-reperfusion injury,” Chin. Med. J. (Engl.), 118, No. 20, 1723–1727 (2005).

    CAS  Google Scholar 

  15. Y. S. Chen, C. T. Chien, M. C. Ma, et al., “Protection ‘outside the box’ (skeletal remote preconditioning) in rat model is triggered by free radical pathway,” J. Surg. Res., 126, No. 1, 92–101 (2005).

    Article  CAS  PubMed  Google Scholar 

  16. M. M. Cheung, R. K. Kharbanda, I. E. Konstantinov, et al., “Randomized controlled trial of the effects of remote ischemic preconditioning on children undergoing cardiac surgery: first clinical application in humans,” J. Am. Coll. Cardiol., 47, No. 11, 2277–2282, (2006).

    Article  PubMed  Google Scholar 

  17. E. W. Dickson, W. A. Porcaro, R. A. Fenton, et al., “’Preconditioning at a distance’ in the isolated rabbit heart,” Acad. Emerg. Med., 7, No. 4, 311–317 (2000).

    Article  CAS  PubMed  Google Scholar 

  18. T. Dohi, A. Maehara, S. J. Brener, et al., “Utility of peak creatine kinase-MB measurements in predicting myocardial infarct size, left ventricular dysfunction, and outcome after first anterior wall acute myocardial infarction (from the INFUSE-AMI trial),” Am. J. Cardiol., 115, No. 5, 563–570 (2015).

    Article  CAS  PubMed  Google Scholar 

  19. M. Donato, B. Buchholz, M. Rodriguez, et al., “Role of the parasympathetic nervous system in cardioprotection by remote hindlimb ischemic preconditioning,” Exp. Physiol., 98, No. 2, 425–434 (2013).

    Article  PubMed  Google Scholar 

  20. J. Dow, A. Bhandari, B. Z. Simkhovich, et al., “The effect of acute versus delayed remote ischemic preconditioning on reperfusion induced ventricular arrhythmias,” J. Cardiovasc. Electrophysiol., 23, No. 12, 1374–1383 (2012).

    Article  PubMed  Google Scholar 

  21. X. Duan, B. Ji, X. Wang, et al., “Expression of microRNA-1 and microRNA-21 in different protocols of ischemic conditioning in an isolated rat heart model,” Cardiology, 122, 36–43 (2012).

    Article  CAS  PubMed  Google Scholar 

  22. N. Erling, N. K. Nakagawa, J. W. Costa Cruz, et al., “Microcirculatory effects of local and remote ischemic preconditioning in supraceliac aortic clamping,” J. Vasc. Surg., 52, No. 5, 1321–1329 (2010).

    Article  PubMed  Google Scholar 

  23. N. Gedik, M. Thielmann, E. Kottenberg, et al., “No evidence for activated autophagy in left ventricular myocardium at early reperfusion with protection by remote ischemic preconditioning in patients undergoing coronary artery bypass grafting,” PLoS One, 9, No. 5, e96567 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  24. B. C. Gho, R. G. Schoemaker, M. A. van den Doel, et al., “Myocardial protection by brief ischemia in noncardiac tissue,” Circulation, 94, No. 9, 2193–2200 (1996).

    Article  CAS  PubMed  Google Scholar 

  25. D. J. Hausenloy, P. K. Mwamure, V. Venugopal, et al., “Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomised controlled trial,” Lancet, 370, No. 9587, 575–579 (2007).

    Article  PubMed  Google Scholar 

  26. M. Heidbreder, A. Naumann, K. Tempel, et al., “Remote vs ischaemic preconditioning: the differential rote of mitogen-activated protein kinase pathways,” Cardiovasc. Res., 78, No. 1, 108–115 (2008).

    Article  CAS  PubMed  Google Scholar 

  27. S. B. Kristiansen, O. Henning, R. K. Kharbanda, et al., “Remote preconditioning reduces ischemic injury in the explanted heart by a KATP channel-dependent mechanism,” Am. J. Physiol. Heart Circ. Physiol., 288, No. 3, H1252–H1256 (2005).

    Article  CAS  PubMed  Google Scholar 

  28. C. Li, Y. S. Li, M. Xu, et al., “Limb remote ischemic preconditioning for intestinal and pulmonary protection during elective open infrarenal abdominal aortic aneurysm repair: a randomized controlled trial,” Anesthesiology, 118, No. 4, 842–852 (2013).

    Article  CAS  PubMed  Google Scholar 

  29. D. A. Liem, P. D. Verdouw, H. Ploeg, et al., “Sites of action of adenosine in interorgan preconditioning of the heart,” Am. J. Physiol. Heart Circ. Physiol., 283, No. 1, H29–H37 (2002).

    Article  CAS  PubMed  Google Scholar 

  30. C. Lotz, M. Lazariotto, A. Redel, et al., “Activation of peroxisome-proliferator-activated receptors α and γ mediates remote ischemic preconditioning against myocardial infarction vivo,” Exp. Biol. Med. (Maywood), 236, No. 1, 113–122 (2011).

    Article  CAS  Google Scholar 

  31. H. L. Lujan and S. E. DiCarlo, “Partial hindlimb occlusion reduced the susceptibility to sustained ventricular tachycardia in conscious rats,” J. Cardiovasc. Pharmacol. Ther., 14, No. 3, 199–206 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  32. T. B. McClanahan, B. S. Nao, L. J. Wolke, et al., “Brief renal occlusion and reperfusion reduces myocardial infarct size in rabbits,” FASEB J., 7, A118.682 (abstract) (1993).

  33. B. W. McCrindle, N. A. Clarizia, S. Khaikin, et al., “Remote ischemic preconditioning in children undergoing cardiac surgery with cardiopulmonary bypass: a single-center double-blinded randomized trial,” J. Am. Heart. Assoc., 3, No. 4, e000964 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  34. M. Murarikova, S. Carnicka, D. Pancza, et al., “Does the remote ischemic preconditioning have an impact on ischemia/reperfusion injury in the isolated diabetic rat heart?” Cardiovasc. Res., 103, Suppl. 1, 438 (2014).

  35. C. E. 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  CAS  PubMed  Google Scholar 

  36. A. Nakano, G. Heusch, M. V. Cohen, and J. M. Downey, “Preconditioning one myocardial region does not necessarily precondition the whole rabbit heart,” Basic Res. Cardiol., 97, No. 1, 35–39 (2002).

    Article  PubMed  Google Scholar 

  37. M. F. Noorbakhsh, H. A. Arab, and H. R. Kazerani, “Liver ischemia preconditions the heart against ischemia-reperfusion arrhythmias,” Iran J. Basic Med. Sci., 18, No. 1, 80–88 (2015).

    PubMed  PubMed Central  Google Scholar 

  38. T. Oxman, M. Arad, R. Klein, et al., “Limb ischemia preconditions the heart against reperfusion tachyarrhythmia,” Am. J. Physiol., 273, No. 4, Pt. 2, H1707–H1712 (1997).

    CAS  PubMed  Google Scholar 

  39. H. H. Patel, J. Moore, A. K. Hsu, and G. J. Gross, “Cardioprotection at a distance: mesenteric artery occlusion protects the myocardium via an opioid sensitive mechanism,” J. Mol. Cell. Cardiol., 34, No. 10, 1317–1323 (2002).

    Article  CAS  PubMed  Google Scholar 

  40. M. A. Pavione, F. Carmona, M. de Castro, and A. P. Carlotti, “Late remote ischemic preconditioning in children undergoing cardiopulmonary bypass: A randomized controlled trial,” J. Thorac. Cardiovasc. Surg., 144, No. 1, 178–183, e1 (2012).

    Article  PubMed  Google Scholar 

  41. T. J. Pell, G. F. Baxter, D. M. Yellon, and G. M. Drew, “Renal ischemia preconditions myocardium: role of adenosine receptors and ATP-sensitive potassium channels,” Am. J. Physiol., 275, No. 5, Pt. 2, H1542–H1547 (1998).

    CAS  PubMed  Google Scholar 

  42. S. Pepe, N. Y. Liaw, M. Hepponstall, et al., “Effect of remote ischemic preconditioning on phosphorylated protein signaling in children undergoing tetralogy of Fallot repair: a randomized controlled trial,” J. Am. Heart Assoc., 2, No. 3, e000095 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  43. N. N. Petrishchev, T. D. Vlasov, V. G. Sipovsky, et al., “Does nitric oxide generation contribute to the mechanism of remote ischemic preconditioning?” Pathophysiology, 7, No. 4, 271–274 (2001).

    Google Scholar 

  44. K. Przyklenk, B. Bauer, M. Ovize, et al., “Regional ischemic ‘preconditioning’ protects remote virgin myocardium from subsequent sustained coronary occlusion,” Circulation, 87, No. 3, 893–899 (1993).

    Article  CAS  PubMed  Google Scholar 

  45. M. H. Rosner, C. Ronco, and M. D. Okusa, “The role of inflammation in the cardio-renal syndrome: a focus on cytokines and inflammatory mediators,” Semin. Nephrol,, 32, No. 1, 70–78 (2012).

    Article  CAS  PubMed  Google Scholar 

  46. J. Sachdeva, W. Dai, P. Z. Gerczuk, and R. A. Kloner, “Combined remote perconditioning and postconditioning failed to attenuate infarct size and contractile dysfunction in a rat model of coronary artery occlusion,” J. Cardiovasc. Pharmacol. Ther., 19, No. 6, 567–573 (2014).

    Article  CAS  PubMed  Google Scholar 

  47. M. R. Schmidt, M. Smerup, I. E. Konstantinov, et al., “Intermittent peripheral tissue ischemia during coronary ischemia reduces myocardial infarction through a KATP-dependent mechanism: first demonstration of remote ischemic perconditioning,” Am. J. Physiol. Heart Circ. Physiol., 292, No. 4, H1883–H1890 (2007).

    Article  CAS  PubMed  Google Scholar 

  48. M. R. Schmidt, N. B. Støttrup, H. Contractor, et al., “Remote ischemic preconditioning with – but not without – metabolic support protects the neonatal porcine heart against ischemia-reperfusion injury,” Int. J. Cardiol., 170, No. 3, 88–393 (2014).

    Article  Google Scholar 

  49. M. R. Schmidt, N. B. Støttrup, M. M. Michelsen, et al., “Remote ischemic preconditioning impairs ventricular function and increases infarct size after prolonged ischemia in the isolated neonatal rabbit heart,” J. Thorac. Cardiovasc. Surg., 147, No. 3, 1049–1055 (2014).

    Article  PubMed  Google Scholar 

  50. R. G. Schoemaker and C. L. van Heijningen, “Bradykinin mediates cardiac preconditioning at a distance,” Am. J. Physiol. Heart Circ. Physiol., 278, No. 5, H1571–H1576 (2000).

    CAS  PubMed  Google Scholar 

  51. M. Shahid, M. Tauseef, K. K. Sharma, and M. Fahim, “Brief femoral artery ischaemia provides protection against myocardial ischemiareperfusion injury in rats: the possible mechanisms,” Exp. Physiol., 93, No. 8, 954–968 (2008).

    Article  CAS  PubMed  Google Scholar 

  52. M. Shimizu, I. E. Konstantinov, R. K. Kharbanda, et al., “Effects of intermittent lower limb ischaemia on coronary blood flow and coronary resistance in pigs,” Acta Physiol. (Oxf.), 190, No. 2, 103–109 (2007).

    Article  CAS  Google Scholar 

  53. M. Shimizu, P. Saxena, I. E. Konstantinov, et al., “Remote ischemic preconditioning decreases adhesion and selectively modifies functional responses of human neutrophils,” J. Surg. Res., 158, No. 1, 155–161 (2010).

    Article  CAS  PubMed  Google Scholar 

  54. D. Singh and K. Chopra, “Evidence of the role of angiotensin AT1 receptors in remote renal preconditioning of myocardium,” Methods Find. Exp. Clin. Pharmacol., 26, No. 2, 117–122 (2004).

    Article  CAS  PubMed  Google Scholar 

  55. M. V. Souza Filho, R. T. Loiola, E. L. Rocha, et al., “Hind limb ischemic preconditioning induces an anti-inflammatory response by remote organs in rats,” Braz. J. Med. Biol. Res., 42, No. 10, 921–929 (2009).

    Article  CAS  PubMed  Google Scholar 

  56. H. Takagi, Y. Matsui, and J. Sadoshima, “The role of autophagy in mediating cell survival and death during ischemia and reperfusion in the heart,” Antioxid. Redox Signal., 9, No. 9, 1373–1382 (2007).

    Article  CAS  PubMed  Google Scholar 

  57. A. Takaoka, I. Nakae, K. Mitsunami, et al., “Renal ischemia/reperfusion remotely improves myocardial energy metabolism during myocardial ischemia via adenosine receptors in rabbits: effects of ‘remote preconditioning,’” J. Am. Coll. Cardiol., 33, No. 2, 556–564 (1999).

    Article  CAS  PubMed  Google Scholar 

  58. R. H. Thiele, J. M. Isbell, and M. H. Rosner, “AKI associated with cardiac surgery,” Clin. J. Am. Soc. Nephrol., 10, No. 3, 500–514 (2015).

    Article  PubMed  Google Scholar 

  59. M. Thielmann, E. Kottenberg, P. Kleinbongard, et al., “Cardioprotective and prognostic effects of remote ischaemic preconditioning in patients undergoing coronary artery bypass surgery: a single-centre randomised, double-blind, controlled trial,” Lancet, 382, No. 9892, 597–604 (2013).

    Article  PubMed  Google Scholar 

  60. A. T. Ulus, S. Yavas, A. Sapmaz, et al., “Effect of conditioning on visceral organs during indirect ischemia/reperfusion injury,” Ann. Vasc. Surg., 28, No. 2, 437–444 (2014).

    Article  PubMed  Google Scholar 

  61. P. D. Verdouw, B. C. Gho, M. M. Koning, et al., “Cardioprotection by ischemic and nonischemic myocardial stress and ischemia in remote organs. Implications for the concept of ischemic preconditioning,” Ann. Acad. Sci., 793, 27–42 (1996).

    Article  CAS  Google Scholar 

  62. C. Voucharas, A. Lazou, F. Triposkiadis, and N. Tsilimingas, “Remote preconditioning in normal and hypertrophic rat hearts,” J. Cardiothorac. Surg., 6, 34 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  63. N. F. Wang, J. Xu, Q. Xia, et al., “Mechanism of cardioprotection induced by noninvasive limb ischemic preconditioning,” Chin. Med. J., 89, No. 28, 1999–2002 (2009).

    Google Scholar 

  64. Y. P. Wang, H. Maeta, K. Mizoguchi, et al., “Intestinal ischemia preconditions myocardium: role of protein kinase C and mitochondrial KATP channel,” Cardiovasc. Res., 55, No. 3, 576–582 (2002).

    Article  CAS  PubMed  Google Scholar 

  65. Z. Wang, Y. Ji, S. Wang, et al., “Protective effect of intestinal ischemic preconditioning on ischemia reperfusion-caused lung injury in rats,” Inflammation, 38, No. 1, 424–432 (2015).

    Article  CAS  PubMed  Google Scholar 

  66. C. Weinbrenner, M. Nelles, N. Herzog, et al., “Remote preconditioning by infrarenal occlusion of the aorta protects the heart from infarction: a newly identified non-neuronal but PKC-dependent pathway,” Cardiovasc. Res., 55, No. 3, 590–601 (2002).

    Article  CAS  PubMed  Google Scholar 

  67. Z. Wenwu, Z. Debing, C. Renwei, et al., “Limb ischemic preconditioning reduces heart and lung injury after an open heart operation in infants,” Pediatr. Cardiol., 31, No. 1, 22–29 (2010).

    Article  Google Scholar 

  68. S. Wolfrum, K. Schneider, M. Heidbreder, et al., “Remote preconditioning protects the heart by activating myocardial PKCε-isoform,” Cardiovasc. Res., 55, No. 3, 583–589 (2002).

    Article  CAS  PubMed  Google Scholar 

  69. R. Q. Xie, W. Cui, Y. M. Hao, et al., “Effects of remote preconditioning induced by skeletal muscle ischemia on myocardial cells apoptosis and roles of opioid receptors in pigs,” Chin. J. Appl. Physiol., 22, No. 4, 474–478 (2006).

    CAS  Google Scholar 

  70. P. Xin, W. Zhu, J. Li, et al., “Combined local ischemic postconditioning and remote perconditioning recapitulate cardioprotective effects of local ischemic preconditioning,” Am. J. Physiol. Heart Circ. Physiol., 298, No. 6, H1819–H1831 (2010).

    Article  CAS  PubMed  Google Scholar 

  71. J. Xu, S. Sun, X. Lu, et al., “Remote ischemic pre- and postconditioning improve postresuscitation myocardial and cerebral function in a rat model of cardiac arrest and resuscitation,” Crit. Care Med., 43, No. 1, e12–e18 (2015).

    Article  PubMed  Google Scholar 

  72. X. Xu, Y. Zhou, S. Luo, et al., “Effect of remote ischemic preconditioning in the elderly patients with coronary artery disease with diabetes mellitus undergoing elective drug-eluting stent implantation,” Angiology, 65, No. 8, 660–666 (2014).

    Article  PubMed  Google Scholar 

  73. W. Zhou, D. Zeng, R. Chen, et al., “Limb ischemic preconditioning reduces heart and lung injury after an open heart operation in infants,” Pediatr. Cardiol., 31, No. 1, 22–29 (2010).

    Article  CAS  PubMed  Google Scholar 

  74. S. B. Zhu, Y. Liu, Y. Zhu, et al., “Remote preconditioning, perconditioning, and postconditioning: a comparative study of their cardio-protective properties in rat models,” Clinics (Sao Paulo) , 68, No. 2, 263–268 (2013)

    Article  Google Scholar 

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Correspondence to L. N. Maslov.

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Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 102, No. 4, pp. 398–410, April, 2016.

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Maslov, L.N., Podoksenov, Y.K., Tsibul’nikov, S.Y. et al. The Phenomenon of Remote Preconditioning of the Heart and Its Main Manifestations . Neurosci Behav Physi 47, 667–674 (2017). https://doi.org/10.1007/s11055-017-0453-8

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