Supercooling enables long-term transplantation survival following 4 days of liver preservation

Nature Medicine

Volumn 20, Issue 7, 2014, Pages 790-793

  Berendsen, Tim A ^a,b   Bruinsma, Bote G ^a   Puts, Catheleyne F ^a   Saeidi, Nima ^a   Usta, O Berk ^a   Uygun, Basak E ^a   Izamis, Maria Louisa ^a   Toner, Mehmet ^a   Yarmush, Martin L ^a,c   Uygun, Korkut ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; GRAFT PERFUSION; GRAFT RECIPIENT; GRAFT SURVIVAL; LIVER CIRRHOSIS; LIVER PRESERVATION; LIVER TRANSPLANTATION; LONG TERM CARE; NONHUMAN; PRIORITY JOURNAL; RAT; ROOM TEMPERATURE; TIME;

RATTUS;

ANIMALS; COLD TEMPERATURE; LIVER TRANSPLANTATION; ORGAN PRESERVATION; RATS; SURVIVAL RATE;

EID: 84904036678     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3588     Document Type: Article

References (43)

1. US Department of Health & Human Services Health Resources and Services Administration. Organ Procurement and Transplantation Network (OPTN), http://optn.transplant.hrsa.gov/ (2014; accessed 1 June 2014).
2. Belzer, F.O. & Southard, J.H. Principles of solid-organ preservation by cold storage. Transplantation 45, 673-676 (1988).
3. Ploeg, R.J. et al. Successful 72-hour cold storage kidney preservation with UW solution. Transplant. Proc. 20, 935-938 (1988).
4. Fahy, G.M. et al. Cryopreservation of organs by vitrification: perspectives and recent advances. Cryobiology 48, 157-178 (2004).
5. Song, Y.C., Khirabadi, B.S., Lightfoot, F., Brockbank, K.G. & Taylor, M.J. Vitreous cryopreservation maintains the function of vascular grafts. Nat. Biotechnol. 18, 296-299 (2000).
6. Fahy, G.M., Wowk, B. & Wu, J. Cryopreservation of complex systems: the missing link in the regenerative medicine supply chain. Rejuvenation Res. 9, 279-291 (2006).
7. Pegg, D.E. The relevance of ice crystal formation for the cryopreservation of tissues and organs. Cryobiology 60, S36-S44 (2010).
8. Rall, W.F. & Fahy, G.M. Ice-free cryopreservation of mouse embryos at -196 °C by vitrification. Nature 313, 573-575 (1985).
9. Fahy, G.M. et al. Physical and biological aspects of renal vitrification. Organogenesis 5, 167-175 (2009).
10. al-Abdulla, N.A. et al. The effects of supercooling chemicals on myocardial ultrastructure: a transmission electron microscopy case study. Conn. Med. 59, 387-399 (1995).
11. Banafsche, R., Pomer, S. & Staehler, G. Nonfreezing cryopreservation - a possible means of improving long-term transplant function? Transpl. Int. 11, 127-136 (1998).
12. Kato, H., Tomita, S., Yamaguchi, S., Ohtake, H. & Watanabe, G. Subzero 24-hr nonfreezing rat heart preservation: a novel preservation method in a variable magnetic field. Transplantation 94, 473-477 (2012).
13. Monzen, K. et al. The use of a supercooling refrigerator improves the preservation of organ grafts. Biochem. Biophys. Res. Commun. 337, 534-539 (2005).
14. Okamoto, T. et al. Successful sub-zero non-freezing preservation of rat lungs at -2 °C utilizing a new supercooling technology. J. Heart Lung Transplant. 27, 1150-1157 (2008).
15. Scotte, M. et al. Liver preservation below 0 °C with UW solution and 2, 3-butanediol. Cryobiology 33, 54-61 (1996).
16. Yoshida, K. et al. A novel conception for liver preservation at a temperature just above freezing point. J. Surg. Res. 81, 216-223 (1999).
17. Ishine, N., Rubinsky, B. & Lee, C.Y. Transplantation of mammalian livers following freezing: vascular damage and functional recovery. Cryobiology 40, 84-89 (2000).
18. Guarrera, J.V. et al. Hypothermic machine preservation in human liver transplantation: the first clinical series. Am. J. Transplant. 10, 372-381 (2010).
19. Moers, C. et al. Machine perfusion or cold storage in deceased-donor kidney transplantation. N. Engl. J. Med. 360, 7-19 (2009).
20. Dutkowski, P., de Rougemont, O. & Clavien, P.A. Machine perfusion for 'Marginal' liver grafts. Am. J. Transplant. 8, 917-924 (2008).
21. Maathuis, M.H. et al. Improved kidney graft function after preservation using a novel hypothermic machine perfusion device. Ann. Surg. 246, 982-988, discussion 989-991 (2007).
22. Nowak, G., Ungerstedt, J., Wernerson, A., Ungerstedt, U. & Ericzon, B.G. Hepatic cell membrane damage during cold preservation sensitizes liver grafts to rewarming injury. J. Hepatobiliary Pancreat. Surg. 10, 200-205 (2003).
23. Usta, O.B. et al. Supercooling as a viable non-freezing cell preservation method of rat hepatocytes. PLo S ONE 8, e69334 (2013).
24. Taylor, M.J. in Advances in Biopreservation (eds. Baust, J.G., Baust, J.M. & Group, F.) Ch. 2 (CRC Press, Boca Raton, Florida, 2007).
25. Gao, W., Bentley, R.C., Madden, J.F. & Clavien, P.A. Apoptosis of sinusoidal endothelial cells is a critical mechanism of preservation injury in rat liver transplantation. Hepatology 27, 1652-1660 (1998).
26. Huet, P.M. et al. Sinusoidal endothelial cell and hepatocyte death following cold ischemia-warm reperfusion of the rat liver. Hepatology 39, 1110-1119 (2004).
27. Schlegel, A., Rougemont, O., Graf, R., Clavien, P.A. & Dutkowski, P. Protective mechanisms of end-ischemic cold machine perfusion in DCD liver grafts. J. Hepatol. 58, 278-286 (2013).
28. Mühlbacher, F., Langer, F. & Mittermayer, C. Preservation solutions for transplantation. Transplant Proc. 31, 2069-2070 (1999).
29. Dutheil, D., Underhaug Gjerde, A., Petit-Paris, I., Mauco, G. & Holmsen, H. Polyethylene glycols interact with membrane glycerophospholipids: is this part of their mechanism for hypothermic graft protection? J. Chem. Biol. 2, 39-49 (2009).
30. Oltean, M. et al. Intraluminal polyethylene glycol stabilizes tight junctions and improves intestinal preservation in the rat. Am. J. Transplant. 12, 2044-2051 (2012).
31. Bessems, M., Doorschodt, B.M., Hooijschuur, O., van Vliet, A.K. & van Gulik, T.M. Optimization of a new preservation solution for machine perfusion of the liver: which is the preferred colloid? Transplant. Proc. 37, 329-331 (2005).
32. Storey, K.B., Bischof, J. & Rubinsky, B. Cryomicroscopic analysis of freezing in liver of the freeze-tolerant wood frog. Am. J. Physiol. 263, R185-R194 (1992).
33. Klepper, J. et al. Erythrocyte 3-O-methyl-d-glucose uptake assay for diagnosis of glucose-transporter-protein syndrome. J. Clin. Lab. Anal. 13, 116-121 (1999).
34. Sugimachi, K., Roach, K.L., Rhoads, D.B., Tompkins, R.G. & Toner, M. Nonmetabolizable glucose compounds impart cryotolerance to primary rat hepatocytes. Tissue Eng. 12, 579-588 (2006).
35. Gok, M.A. et al. Improving the quality of kidneys from non-heart-beating donors, using streptokinase: an animal model. Transplantation 73, 1869-1874 (2002).
36. Minor, T. & Paul, A. Hypothermic reconditioning in organ transplantation. Curr. Opin. Organ Transplant. 18, 161-167 (2013).
37. Vogel, T., Brockmann, J.G. & Friend, P.J. Ex vivo normothermic liver perfusion: an update. Curr. Opin. Organ Transplant. 15, 167-172 (2010).
38. Berendsen, T.A. et al. A simplified subnormothermic machine perfusion system restores ischemically damaged liver grafts in a rat model of orthotopic liver transplantation. Transplant. Res. 1, 6 (2012).
39. Bruinsma, B.G. et al. Subnormothermic machine perfusion for ex vivo preservation and recovery of the human liver for transplantation. Am. J. Transplant. 14, 1400-1409 (2014).
40. Bruinsma, B.G., Berendsen, T.A., Izamis, M.L., Yarmush, M.L. & Uygun, K. Determination and extension of the limits to static cold storage using subnormothermic machine perfusion. Int. J. Artif. Organs 36, 775-780 (2013).
41. Tolboom, H. et al. A model for normothermic preservation of the rat liver. Tissue Eng. 13, 2143-2151 (2007).
42. Tolboom, H. et al. Recovery of warm ischemic rat liver grafts by normothermic extracorporeal perfusion. Transplantation 87, 170-177 (2009).
43. Izamis, M.-L. et al. Simple machine perfusion significantly enhances hepatocyte yields of ischemic and fresh rat livers. Cell Med. 4, 109-123 (2013).