Remote ischaemic conditioning - Therapeutic opportunities in renal medicine

Nature Reviews Nephrology

Volumn 9, Issue 12, 2013, Pages 739-746

  Crowley, Lisa E ^a   McIntyre, Christopher W ^b  

^a ROYAL DERBY HOSPITAL   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; G PROTEIN COUPLED RECEPTOR; GLYCOGEN SYNTHASE KINASE 3BETA; HEAT SHOCK PROTEIN 27; MITOGEN ACTIVATED PROTEIN KINASE 1; NITRIC OXIDE SYNTHASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; S6 KINASE;

ACUTE HEART INFARCTION; ACUTE KIDNEY FAILURE; CARDIOVASCULAR FUNCTION; CARDIOVASCULAR MORTALITY; CAROTID ENDARTERECTOMY; CHRONIC KIDNEY DISEASE; CHRONIC KIDNEY FAILURE; CONGESTIVE HEART FAILURE; CONTRAST INDUCED NEPHROPATHY; CORONARY ARTERY BYPASS SURGERY; DIABETES MELLITUS; FOLLOW UP; HEART FUNCTION; HEART INFARCTION; HEART INJURY; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE INJURY; HEART MUSCLE REPERFUSION; HEART PROTECTION; HEMODYNAMIC STRESS; HUMAN; HYPERLIPIDEMIA; HYPERTENSION; ISCHEMIC POSTCONDITIONING; ISCHEMIC PRECONDITIONING; KIDNEY FAILURE; MESENTERIC ARTERY; META ANALYSIS (TOPIC); MITOCHONDRION SWELLING; NEUROPATHY; OXIDATIVE STRESS; PERCUTANEOUS CORONARY INTERVENTION; PRIORITY JOURNAL; QUALITY OF LIFE; RANDOMIZED CONTROLLED TRIAL (TOPIC); REMOTE ISCHEMIC CONDITIONING; RENAL ARTERY; RENAL REPLACEMENT THERAPY; REPERFUSION INJURY; REVIEW; ST SEGMENT ELEVATION MYOCARDIAL INFARCTION; STUNNED HEART MUSCLE; SUDDEN CARDIAC DEATH; SYSTEMATIC REVIEW (TOPIC);

ACUTE KIDNEY INJURY; BLOOD UREA NITROGEN; CONTRAST MEDIA; CREATININE; HUMANS; ISCHEMIC POSTCONDITIONING; ISCHEMIC PRECONDITIONING; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RENAL DIALYSIS; RENAL INSUFFICIENCY, CHRONIC; REPERFUSION INJURY;

EID: 84888876817     PISSN: 17595061     EISSN: 1759507X     Source Type: Journal    
DOI: 10.1038/nrneph.2013.226     Document Type: Review

References (79)

1. Carden, D. L. & Granger D. N. Pathophysiology of ischaemia- reperfusion injury. J. Pathol. 190, 255-266 (2000) (Pubitemid 30141372)
2. Murry, C. E., Jennings, R. B. & Reimer, K. A. Preconditioning with ischemia - a delay of lethal cell injury in ischemic myocardium. Circulation 74, 1124-1136 (1986) (Pubitemid 17174962)
3. Hausenloy, D. J. & Yellon, D. M. Preconditioning and postconditioning: underlying mechanisms and clinical application. Atherosclerosis 204, 334-341 (2009)
4. Marber, M. S., Latchman, D. S., Walker, J. M., & Yellon, D. M. Cardiac stress protein elevation 24 hours after brief ischemia or heat-stress is associated with resistance to myocardial-infarction. Circulation 88, 1264-1272 (1993) (Pubitemid 23264047)
5. Wang, N. P., Wang, Z. F., Philip, T. & Zhao, Z. Q. Sr. Inhibition of adverse myocardial remodeling and improvement of cardiac function with postconditioning: comparison with preconditioning [abstract]. Circulation 124, A9579 (2011)
6. Gho, B. C. G., Schoemaker, R. G., van den Doel, M. A., Duncker, D. J. & Verdouw, P. D. Myocardial protection by brief ischemia in noncardiac tissue. Circulation 94, 2193-2200 (1996) (Pubitemid 26360513)
7. Birnbaum, Y., Hale, S. L. & Kloner, R. A. Ischemic preconditioning at a distance: Reduction of myocardial infarct size by partial reduction of blood supply combined with pacing of the gastrocnemius muscle in the rabbit. Circulation 96, 1641-1646 (1997) (Pubitemid 27375364)
8. Loukogeorgakis, S. P. et al. Remote ischemic preconditioning provides early and late protection against endothelial ischemia-reperfusion injury in humans: Role of the autonomic nervous system. J. Am. Coll. Cardiol. 46, 450-456 (2005) (Pubitemid 41040285)
9. Schmidt, M. R. et al. Intermittent peripheral tissue ischemia during coronary ischemia reduces myocardial infarction through a KATPdependent mechanism: first demonstration of remote ischemic perconditioning. Am. J. Physiol. Heart. Circ. Physiol. 292, H1883-H1890 (2007) (Pubitemid 46572412)
10. Botker, H. E. et al. Remote ischaemic conditioning before hospital admission, as a complement to angioplasty, and effect on myocardial salvage in patients with acute myocardial infarction: A randomised trial. Lancet 375, 727-734 (2010)
11. Rentoukas, I. et al. Cardioprotective role of remote ischemic periconditioning in primary percutaneous coronary intervention enhancement by opioid action. JACC Cardiovasc. Interv. 3, 49-55 (2010)
12. Garlid, K. D., Costa, A. D. T., Quinlan, C. L., Pierre, S. V. & Dos Santos, P. Cardioprotective signaling to mitochondria. J. Mol. Cell. Cardiol. 46, 858-866 (2009)
13. Shi, W. W. & Vinten-Johansen, J. Endogenous cardioprotection by ischaemic postconditioning and remote conditioning. Cardiovasc. Res. 94, 206-216 (2012)
14. Heusch, G. et al. STAT5 activation and cardioprotection by remote ischemic preconditioning in humans. Circ. Res. 110, 111-115 (2012)
15. Shimizu, M. et al. Transient limb ischaemia remotely preconditions through a humoral mechanism acting directly on the myocardium: Evidence suggesting cross-species protection. Clin. Sci. (Lond.) 117, 191-200 (2009)
16. Baxter, G. F. Role of adenosine in delayed preconditioning of myocardium. Cardiovasc. Res. 55, 483-494 (2002) (Pubitemid 34874943)
17. Park, K. M. et al. Inducible nitric-oxide synthase is an important contributor to prolonged protective effects of ischemic preconditioning in the mouse kidney. J. Biol. Chem. 278, 27256-27266 (2003) (Pubitemid 36876883)
18. Ding, Y. K., Zhang, M. M. & He, R. R. Role of renal nerve in cardioprotection provided by renal ischaemic preconditioning in anaesthetized rabbits. Sheng Li Xue Bao. 53, 7-12 (2001)
19. Oosterlinck, W. et al. Diabetes mellitus and the metabolic syndrome do not abolish, but might reduce, the cardioprotective effect of ischemic postconditioning. J. Thorac. Cardiovasc. Surg. 145, 1595-1602 (2013)
20. Engbersen, R. et al. Improved resistance to ischemia and reperfusion, but impaired protection by ischemic preconditioning in patients with type 1 diabetes mellitus: A pilot study. Cardiovasc. Diabetol. 11, 124 (2012)
21. Konstantinov, I. E. et al. Remote ischemic preconditioning of the recipient reduces myocardial ischemia-reperfusion injury of the denervated donor heart via a KATP channel-dependent mechanism. Transplantation 79, 1691-1695 (2005) (Pubitemid 40885266)
22. Lim, S. Y., Yellon, D. M. & Hausenloy, D. J. The neural and humoral pathways in remote limb ischemic preconditioning. Basic Res. Cardiol. 105, 651-655 (2010)
23. Hausenloy, D. J. & Yellon, D. M. Reperfusion injury salvage kinase signalling: taking a RISK for cardioprotection. Heart Fail. Rev. 12, 217-234 (2007) (Pubitemid 350176695)
24. Jenkins, D. P. et al. Ischaemic preconditioning reduces troponin T release in patients undergoing coronary artery bypass surgery. Heart 77, 314-318 (1997) (Pubitemid 27208169)
25. Hoole, S. P. et al. Cardiac remote ischemic preconditioning in coronary stenting (CRISP Stent) study a prospective, randomized control trial. Circulation 119, 820-827 (2009)
26. Luo, W. J., Li, B., Lin, G. Q. & Huang, R. M. Postconditioning in cardiac surgery for tetralogy of Fallot. J. Thorac. Cardiovasc. Surg. 133, 1373-1374 (2007) (Pubitemid 46635534)
27. Luo, W. J., Li, B., Chen, R., Huang, R. M. & Lin, G. Q. Effect of ischemic postconditioning in adult valve replacement. Eur. J. Cardiothorac. Surg. 33, 203-208 (2008)
28. Luo, W. J., Li, B., Lin, G. Q., Chen, R. & Huang, R. M. Does cardioplegia leave room for postconditioning in paediatric cardiac surgery? Cardiol. Young 18, 282-287 (2008) (Pubitemid 351780775)
29. Lonborg, J. et al. Cardioprotective effects of ischemic postconditioning in patients treated with primary percutaneous coronary intervention, evaluated by magnetic resonance. Circ. Cardiovasc. Interv. 3, 34-41 (2010)
30. Zhao, C. M. et al. Effect of ischaemic postconditioning on recovery of left ventricular contractile function after acute myocardial infarction. J. Int. Med. Res. 40, 1082-1088 (2012)
31. Prasad, A. et al. Remote ischemic preconditioning immediately before percutaneous coronary intervention does not impact myocardial necrosis, inflammatory response, and circulating endothelial progenitor cell counts: A single center randomized sham controlled trial. Catheter Cardiovasc. Interv. 81, 930-936 (2013)
32. Lomivorotov, V. V. et al. Remote ischaemic preconditioning does not protect the heart in patients undergoing coronary artery bypass grafting. Interact. Cardiovasc. Thorac. Surg. 15, 18-22 (2012)
33. Jensen, H. A. et al. Remote ischemic preconditioning protects the brain against injury after hypothermic circulatory arrest. Circulation 123, 714-721 (2011)
34. Walsh, S. R. et al. Remote ischemic preconditioning for cerebral and cardiac protection during carotid endarterectomy: Results from a pilot randomized clinical trial. Vasc. Endovascular Surg. 44, 434-439 (2010)
35. Harder, Y. et al. An old dream revitalised: preconditioning strategies to protect surgical flaps from critical ischaemia and ischaemia-reperfusion injury. J. Plast. Reconstr. Aesthet. Surg. 61, 503-511 (2008) (Pubitemid 351635904)
36. Wang, W. Z., Baynosa, R. C. & Zamboni, W. A. Update on ischemia-reperfusion injury for the plastic surgeon: 2011. Plast. Reconstr. Surg. 128, 685e-692e (2011)
37. Kraemer, R. et al. Acute effects of remote ischemic preconditioning on cutaneous microcirculation - a controlled prospective cohort study. BMC Surg. 11, 32 (2011)
38. Kanoria, S. et al. Remote preconditioning improves hepatic oxygenation after ischaemia reperfusion injury. Transpl. Int. 25, 783-791 (2012)
39. Abu-Amara, M. et al. The hepatic soluble guanylyl cyclase-cyclic guanosine monophosphate pathway mediates the protection of remote ischemic preconditioning on the microcirculation in liver ischemia-reperfusion injury. Transplantation 93, 880-886 (2012)
40. Bobryshev, P., Bagaeva, T. & Filaretova, L. Ischemic preconditioning attenuates gastric ischemia-reperfusion injury through involvement of glucocorticoids. J. Physiol. Pharmacol. 60, 155-160 (2009)
41. Wever, K. E. et al. Ischemic preconditioning in the animal kidney, a systematic review and meta-analysis. PLoS ONE 7, e32296 (2012)
42. Ishihara, M. et al. Diabetes mellitus prevents ischemic preconditioning in patients with a first acute anterior wall myocardial infarction. J. Am. Coll. Cardiol. 38, 1007-1011 (2001) (Pubitemid 32912703)
43. van den Munckhof, I. et al. Aging attenuates the protective effect of ischemic preconditioning against endothelial ischemia-reperfusion injury in humans. Am. J. Physiol. Heart. Circ. Physiol. 304, H1727-H1732 (2013)
44. Vinten-Johansen, J. & Shi, W. W. Perconditioning and postconditioning: current knowledge, knowledge gaps, barriers to adoption, and future directions. J. Cardiovasc. Pharmacol. Ther. 16, 260-266 (2011)
45. Byrne, C. J. et al. Ischemic conditioning protects the uremic heart in a rodent model of myocardial infarction. Circulation 125, 1256-1265 (2012)
46. Kocsis, G. F. et al. Preconditioning protects the heart in a prolonged uremic condition. Am. J. Physiol. Heart Circ. Physiol. 303, H1229-H1236 (2012)
47. Zimmerman, R. F. et al. Ischemic preconditioning at a remote site prevents acute kidney injury in patients following cardiac surgery. Kidney Int. 80, 861-867 (2011)
48. Li, L., Li, G. L., Yu, C. & Li, Y. The role of remote ischemic preconditioning on postoperative kidney injury in patients undergoing cardiac and vascular interventions: A meta-analyses. J. Cardiothorac. Surg. 8, 43 (2013)
49. Huang, Z. Y. et al. Synergy of isoflurane preconditioning and propofol postconditioning reduces myocardial reperfusion injury in patients. Clin. Sci. (Lond.) 121, 57-69 (2011)
50. Er, F. et al. Ischemic preconditioning for prevention of contrast medium-induced nephropathy randomized pilot RenPro trial (Renal Protection Trial). Circulation 126, 296-303 (2012)
51. Jardine, A. G., Gaston, R. S., Fellstrom, B. C. & Holdaas, H. Prevention of cardiovascular disease in adult recipients of kidney transplants. Lancet 378, 1419-1427 (2011)
52. Baigent, C., Burbury, K. & Wheeler, D. Premature cardiovascular disease in chronic renal failure. Lancet 356, 147-152 (2000) (Pubitemid 30438520)
53. McIntyre, C. W. Effects of hemodialysis on cardiac function. Kidney Int. 76, 371-375 (2009)
54. Hajhosseiny, R., Khavandi, K. & Goldsmith, D. J. Cardiovascular disease in chronic kidney disease: untying the Gordian knot. Int. J. Clin. Pract. 67, 14-31 (2013)
55. McIntyre, C. W. Haemodialysis-induced myocardial stunning in chronic kidney disease - a new aspect of cardiovascular disease. Blood Purif. 29, 105-110 (2010)
56. Burton, J. O., Jefferies, H. J., Selby, N. M. & McIntyre, C. W. Hemodialysis-induced repetitive myocardial injury results in global and segmental reduction in systolic cardiac function. Clin. J. Am. Soc. Nephrol. 4, 1925-1931 (2009)
57. Burton, J. O., Jefferies, H. J., Selby, N. M. & McIntyre, C. W. Hemodialysis-induced cardiac injury: determinants and associated outcomes. Clin. J. Am. Soc. Nephrol. 4, 914-920 (2009)
58. McIntyre, C. W. Recurrent circulatory stress: the dark side of dialysis. Sem. Dial. 23, 449-451 (2010)
59. Kotanko, P., Carter, M. & Levin, N. W. Intestinal bacterial microflora - a potential source of chronic inflammation in patients with chronic kidney disease. Nephrol. Dial. Transplant. 21, 2057-2060 (2006) (Pubitemid 44295025)
60. Harrison, L. E. A., Burton, J. O., Szeto, C. C., Li, P. K. T. & McIntyre, C. W. Endotoxaemia in haemodialysis: A novel factor in erythropoetin resistance? PLoS ONE 7, e40209 (2012)
61. Charalambous, B. M., Stephens, R. C. M., Feavers, I. M. & Montgomery, H. E. Role of bacterial endotoxin in chronic heart failure: the gut of the matter. Shock 28, 15-23 (2007) (Pubitemid 46956457)
62. McIntyre, C. W. et al. Circulating endotoxemia: A novel factor in systemic inflammation and cardiovascular disease in chronic kidney disease. Clin. J. Am. Soc. Nephrol. 6, 133-141 (2011)
63. Agganis, B. T. et al. Depression and cognitive function in maintenance hemodialysis patients. Am. J. Kidney Dis. 56, 704-712 (2010)
64. Eldehni, M. T. & McIntyre, C. W. Are there neurological consequences of recurrent intradialytic hypotension? Sem. Dial. 25, 253-256 (2012)
65. Selby, N. M., Burton, J. O., Chesterton, L. F. & McIntyre, C. W. Dialysis-induced regional left ventricular dysfunction is ameliorated by cooling the dialysate. Clin. J. Am. Soc. Nephrol. 1, 1216-1225 (2006)
66. Selby, N. M., Lambie, S. H., Camici, P. G., Baker, C. S. & McIntyre, C. W. Occurrence of regional left ventricular dysfunction in patients undergoing standard and biofeedback dialysis. Am. J. Kidney Dis. 47, 830-841 (2006)
67. Jefferies, H. J., Virk, B., Schiller, B., Moran, J. & McIntyre, C. W. Frequent hemodialysis schedules are associated with reduced levels of dialysis-induced cardiac injury (myocardial stunning). Clin. J. Am. Soc. Nephrol. 6, 1326-1332 (2011)
68. Go, A. S., Chertow, G. M., Fan, D. J., McCulloch, C. E. & Hsu, C. Y. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N. Engl. J. Med. 351, 1296-1305 (2004)
69. Foley, R. N., Parfrey, P. S. & Sarnak, M. J. Clinical epidemiology of cardiovascular disease in chronic renal disease. Am. J. Kidney Dis. 32, S112-S119 (1998) (Pubitemid 28527268)
70. Genovesi, S. et al. Sudden death and associated factors in a historical cohort of chronic haemodialysis patients. Nephrol. Dial. Transplant. 24, 2529-2536 (2009)
71. Kahn, M. R., Robbins, M. J., Kim, M. C. & Fuster, V. Management of cardiovascular disease in patients with kidney disease. Nat. Rev. Cardiol. 10, 261-273 (2013)
72. Odudu, A., Eldehni, M. T., Fakis, A. & McIntyre, C. W. Rationale and design of a multi-centre randomised controlled trial of individualised cooled dialysate to prevent left ventricular systolic dysfunction in haemodialysis patients. BMC Nephrol. 13, 45 (2012)
73. Selby, N. M., Taal, M. W. & McIntyre, C. W. Comparison of progressive conductivity reduction with diacontrol and standard dialysis. ASAIO J. 53, 194-200 (2007) (Pubitemid 46597569)
74. Controlled Trials. Randomised controlled trial of remote ischaemic pre-conditioning to reduce dialysis induced myocardial stunning in haemodialysis patients [online], http://www.controlled-trials.com/isrctn/pf/22392984 (2011)
75. Moro, L., Pedone, C., Mondi, A., Nunziata, E. & Incalzi, R. A. Effect of local and remote ischemic preconditioning on endothelial function in young people and healthy or hypertensive elderly people. Atherosclerosis 219, 750-752 (2011)
76. Dubin, R. F. et al. Association of segmental wall motion abnormalities occurring during hemodialysis with post-dialysis fatigue. Nephrol. Dial. Transplant. 28, 2580-2585 (2013)
77. Cheung, M. M. H. 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, 2277-2282 (2006) (Pubitemid 43795071)
78. Choi, Y. S. et al. Effect of remote ischemic preconditioning on renal dysfunction after complex valvular heart surgery: A randomized controlled trial. J. Thorac. Cardiovasc. Surg. 142, 148-154 (2011)
79. Ren, C. et al. Delayed postconditioning protects against focal ischemic brain injury in rats. PLoS ONE 3, e3851 (2008)