Avoidance of Profound Hypothermia during Initial Reperfusion Improves the Functional Recovery of Hearts Donated after Circulatory Death

American Journal of Transplantation

Volumn 16, Issue 3, 2016, Pages 773-782

  White, C W ^a,b   Ambrose, E ^a,b   Muller A ^c   Li, Y ^b   Le, H ^b   Thliveris, J ^a   Arora, R C ^a,b   Lee, T W ^a   Dixon, I M C ^a,b   Tian, G ^a,d   Nagendran, J ^c   Hryshko, L V ^a,b   Freed, D H ^a,b,c  

^a UNIVERSITY OF MANITOBA   (Canada)

^b St Boniface Research Centre   (Canada)

^c UNIVERSITY OF ALBERTA   (Canada)

^d NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; LIDOCAINE; TROPONIN I;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; ELECTRON MICROSCOPY; ENDOTHELIUM CELL; EXPERIMENTAL PIG; HEART ARREST; HEART DEATH; HEART FUNCTION; HEART MUSCLE INJURY; HEART PERFUSION; NONHUMAN; PRIORITY JOURNAL; PROFOUND INDUCED HYPOTHERMIA; PROTEIN BLOOD LEVEL; TEMPERATURE; ANIMAL; CONVALESCENCE; HEART; HEART MUSCLE REPERFUSION; HEART TRANSPLANTATION; HYPOTHERMIA; MYOCARDIAL ISCHEMIA; ORGAN PRESERVATION; PHYSIOLOGY; PIG; PROCEDURES; TRANSPLANTATION;

ANIMALS; HEART; HEART ARREST, INDUCED; HEART TRANSPLANTATION; HYPOTHERMIA; MYOCARDIAL ISCHEMIA; MYOCARDIAL REPERFUSION; ORGAN PRESERVATION; RECOVERY OF FUNCTION; SWINE; TISSUE AND ORGAN HARVESTING;

EID: 84959494288     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.13574     Document Type: Article

References (47)

1. Shemie SD, Baker AJ, Knoll G, et al., National recommendations for donation after cardiocirculatory death in Canada: Donation after cardiocirculatory death in Canada. CMAJ 2006; 175: S1-S24.
2. Gomez L, Li B, Mewton N, et al., Inhibition of mitochondrial permeability transition pore opening: Translation to patients. Cardiovasc Res 2009; 83: 226-233.
3. Murphy E, Steenbergen C., Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev 2008; 88: 581-609.
4. Sanada S, Komuro I, Kitakaze M., Pathophysiology of myocardial reperfusion injury: Preconditioning, postconditioning, and translational aspects of protective measures. Am J Physiol Heart Circ Physiol 2011; 301: H1723-H1741.
5. Longnus SL, Mathys V, Dornbierer M, Dick F, Carrel TP, Tevaearai HT., Heart transplantation with donation after circulatory determination of death. Nat Rev Cardiol 2014; 11: 354-363.
6. Rosenbaum DH, Peltz M, Merritt ME, Thatcher JE, Sasaki H, Jessen ME., Benefits of perfusion preservation in canine hearts stored for short intervals. J Surg Res 2007; 140: 243-249.
7. Iyer A, Gao L, Doyle A, et al., Increasing the tolerance of DCD hearts to warm ischemia by pharmacological postconditioning. Am J Transplant 2014; 14: 1744-1752.
8. Kotani Y, Ishino K, Osaki S, et al., Efficacy of MCI-186, a free-radical scavenger and antioxidant, for resuscitation of nonbeating donor hearts. J Thorac Cardiovasc Surg 2007; 133: 1626-1632.
9. Scheule AM, Jost D, Beierlein W, et al., Sodium-hydrogen inhibitor cariporide (HOE 642) improves in situ protection of hearts from non-heart-beating donors. J Heart Lung Transplant 2003; 22: 1335-1342.
10. Repse S, Pepe S, Anderson J, McLean C, Rosenfeldt FL., Cardiac reanimation for donor heart transplantation after cardiocirculatory death. J Heart Lung Transplant 2010; 29: 747-755.
11. Dhital KK, Iyer A, Connellan M, et al., Adult heart transplantation with distant procurement and ex-vivo preservation of donor hearts after circulatory death: a case series. Lancet 2015; doi: 10.1016/S0140-6736(15)60038-1 [Epub ahead of print].
12. Osaki S, Ishino K, Kotani Y, et al., Resuscitation of non-beating donor hearts using continuous myocardial perfusion: The importance of controlled initial reperfusion. Anna Thorac Surg 2006; 81: 2167-2171.
13. Siegmund B, Klietz T, Schwartz P, Piper HM., Temporary contractile blockade prevents hypercontracture in anoxic-reoxygenated cardiomyocytes. Am J Physiol 1991; 260: H426-H435.
14. Larsen T, Solberg S, Johansen R, Jorgensen L., Effect of cooling on the intracellular concentrations of Na+, K+ and Cl- in cultured human endothelial cells. Scand J Clin Lab Invest 1988; 48: 565-571.
15. Parolari A, Rubini P, Cannata A, et al., Endothelial damage during myocardial preservation and storage. Ann Thorac Surg 2002; 73: 682-690.
16. Smulowitz PB, Serna DL, Beckham GE, Milliken JC., Ex vivo cardiac allograft preservation by continuous perfusion techniques. ASAIO J 2000; 46: 389-396.
17. Ko T, Otani H, Imamura H, Omori K, Inagaki C., Role of sodium pump activity in warm induction of cardioplegia combined with reperfusion of oxygenated cardioplegic solution. J Thorac Cardiovasc Surg 1995; 110: 103-110.
18. White CW, Ali A, Hasanally D, et al., A cardioprotective preservation strategy employing ex vivo heart perfusion facilitates successful transplant of donor hearts after cardiocirculatory death. J Heart Lung Transplant 2013; 32: 734-743.
19. Rudd DM, Dobson GP., Eight hours of cold static storage with adenosine and lidocaine (Adenocaine) heart preservation solutions: Toward therapeutic suspended animation. J Thorac Cardiovasc Surg 2011; 142: 1552-1561.
20. Allen BS, Okamoto F, Buckberg GD, et al., Reperfusate composition: Benefits of marked hypocalcemia and diltiazem on regional recovery. J Thorac Cardiovasc Surg 1986; 92: 564-572.
21. White CW, Hasanally D, Mundt P, et al., A whole blood-based perfusate provides superior preservation of myocardial function during ex vivo heart perfusion. J Heart Lung Transplant 2015; 34: 113-121.
22. Okamoto K, Kunitomo R, Tagami H, et al., Resuscitation and evaluation of non-beating hearts obtained from asphyxiated dogs via autoperfusing heart-lung circuit. Ann Thorac cardiovascular surgery 2001; 7: 341-345.
23. Iyer A, Gao L, Doyle A, et al., Normothermic ex vivo perfusion provides superior organ preservation and enables viability assessment of hearts from DCD donors. Am J Transplant 2015; 15: 371-380.
24. Izzi G, Zile MR, Gaasch WH., Myocardial oxygen consumption and the left ventricular pressure-volume area in normal and hypertrophic canine hearts. Circulation 1991; 84: 1384-1392.
25. Buckberg GD, Brazier JR, Nelson RL, Goldstein SM, McConnell DH, Cooper N., Studies of the effects of hypothermia on regional myocardial blood flow and metabolism during cardiopulmonary bypass. I. The adequately perfused beating, fibrillating, and arrested heart. J Thorac Cardiovasc Surg 1977; 73: 87-94.
26. Matsumoto T, Miura T, Miki T, Genda S, Shimamoto K., Blockade of the Na+-Ca2+ exchanger is more efficient than blockade of the Na+-H+ exchanger for protection of the myocardium from lethal reperfusion injury. Cardiovasc Drugs Ther 2002; 16: 295-301.
27. Koike N, Takeyoshi I, Ohki S, Tokumine M, Matsumoto K, Morishita Y., Effects of adding P38 mitogen-activated protein-kinase inhibitor to celsior solution in canine heart transplantation from non-heart-beating donors. Transplantation 2004; 77: 286-292.
28. Hearse DJ, Humphrey SM, Chain EB., Abrupt reoxygenation of the anoxic potassium-arrested perfused rat heart: A study of myocardial enzyme release. J Mol Cell Cardiol 1973; 5: 395-407.
29. Piper HM, Abdallah Y, Schafer C., The first minutes of reperfusion: A window of opportunity for cardioprotection. Cardiovasc Res 2004; 61: 365-371.
30. Follette DM, Steed DL, Foglia RP, Fey KH, Buckberg GD., Reduction of postischemic myocardial damage by maintaining arrest during initial reperfusion. Surg Forum 1977; 28: 281-283.
31. Rose DM, Barnhart GR, Jones M., Does secondary cardioplegia provide long-term recovery from ischemic injury ? Ann Thorac Surg 1983; 35: 79-86.
32. Rosenkranz ER, Vinten-Johansen J, Buckberg GD, Okamoto F, Edwards H, Bugyi H., Benefits of normothermic induction of blood cardioplegia in energy-depleted hearts, with maintenance of arrest by multidose cold blood cardioplegic infusions. J Thorac Cardiovasc Surg 1982; 84: 667-677.
33. Beyersdorf F., The use of controlled reperfusion strategies in cardiac surgery to minimize ischaemia/reperfusion damage. Cardiovasc Res 2009; 83: 262-268.
34. Follette DM, Fey K, Buckberg GD, et al., Reducing postischemic damage by temporary modification of reperfusate calcium, potassium, pH, and osmolarity. J Thorac Cardiovasc Surg 1981; 82: 221-238.
35. Jacobs S, Rega F, Meyns B., Current preservation technology and future prospects of thoracic organs. Part 2: heart. Curr Opin Organ Transplant 2010; 15: 156-159.
36. Quentin E, Averet N, Guerin B, Rigoulet M., Temperature dependence of the coupling efficiency of rat liver oxidative phosphorylation: Role of adenine nucleotide translocator. Biochem Biophys Res Commun 1994; 202: 816-821.
37. Kawasuji M, Tomita S, Yasuda T, Sakakibara N, Takemura H, Watanabe Y., Myocardial oxygenation during terminal warm blood cardioplegia. Ann Thorac Surg 1998; 65: 1260-1264.
38. Nomura F, Forbess JM, Mayer EJ., Effects of Hot shot on recovery after hypothermic ischemia in neonatal lamb heart. J Cardiovasc Surg (Torino) 2001; 42: 1-7.
39. Metzdorff MT, Grunkemeier GL, Starr A., Effect of initial reperfusion temperature on myocardial preservation. J Thorac Cardiovasc Surg 1986; 91: 545-550.
40. Luo WJ, Chen SX, Jian HH, Xu LM., A comparison of ischemic preconditioning versus terminal warm cardioplegia with controlled reperfusion in open heart operation. J Cardiovasc Surg (Torino) 2001; 42: 193-196.
41. Toyoda Y, Yamaguchi M, Yoshimura N, Oka S, Okita Y., Cardioprotective effects and the mechanisms of terminal warm blood cardioplegia in pediatric cardiac surgery. J Thorac Cardiovasc Surg 2003; 125: 1242-1251.
42. Osaki S, Ishino K, Kotani Y, et al., Circulatory load during hypoxia impairs post-transplant myocardial functional recovery in donation after cardiac death. J Heart Lung Transplant 2009; 28: 266-272.
43. Hirota M, Ishino K, Fukumasu I, et al., Prediction of functional recovery of 60-minute warm ischemic hearts from asphyxiated canine non-heart-beating donors. J Heart Lung Transplant 2006; 25: 339-344.
44. Fedalen PA, Piacentino V 3rd, Jeevanandam V, et al., Pharmacologic pre-conditioning and controlled reperfusion prevent ischemia-reperfusion injury after 30 minutes of hypoxia/ischemia in porcine hearts. J Heart Lung Transplant 2003; 22: 1234-1244.
45. Labow RS, Hendry PJ, Meek E, Keon WJ., Temperature affects human cardiac sarcoplasmic reticulum energy-mediated calcium transport. J Mol Cell Cardiol 1993; 25: 1161-1170.
46. Diestel A, Billecke N, Roessler J, et al., Methylprednisolone and tacrolimus prevent hypothermia-induced endothelial dysfunction. J Heart Lung Transplant 2009; 28: 718-724.
47. Valantine HA., Cardiac allograft vasculopathy: Central role of endothelial injury leading to transplant "atheroma." Transplantation 2003; 76: 891-899.