State of Art: Clinical ex vivo lung perfusion: Rationale, current status, and future directions

Journal of Heart and Lung Transplantation

Volumn 31, Issue 4, 2012, Pages 339-348

  Sanchez, Pablo G ^a   Bittle, Gregory J ^a   Burdorf, Lars ^a   Pierson III, Richard N ^a   Griffith, Bartley P ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

ex vivo lung perfusion; isolated lung perfusion; lung mechanics; lung metabolism; lung transplantation

Indexed keywords

2 [4 (2 CARBOXYETHYL)PHENETHYLAMINO]ADENOSINE 5' (N ETHYLCARBOXAMIDE); INTERLEUKIN 10; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BACTERIAL LOAD; BLOOD VESSEL PERMEABILITY; CLINICAL TRIAL (TOPIC); CYTOKINE RELEASE; DETERIORATION; EX VIVO STUDY; FLOW RATE; GENE THERAPY; HEALTH CARE PERSONNEL; HEART DEATH; HUMAN; ISOLATED LUNG; LUNG ALVEOLUS EPITHELIUM; LUNG ARTERY PRESSURE; LUNG CIRCULATION; LUNG COMPLIANCE; LUNG EDEMA; LUNG FUNCTION; LUNG INJURY; LUNG MECHANICS; LUNG PERFUSION; LUNG PRESSURE; LUNG TRANSPLANTATION; LUNG VENTILATION; MESENCHYMAL STEM CELL; METABOLIC ACTIVATION; NONHUMAN; ORGAN DONOR; ORGAN PRESERVATION; PRIORITY JOURNAL; VENTILATOR INDUCED LUNG INJURY;

EXTRACORPOREAL CIRCULATION; HUMANS; LUNG; LUNG TRANSPLANTATION; ORGAN PRESERVATION; PERFUSION; REGIONAL BLOOD FLOW;

EID: 84858313699     PISSN: 10532498     EISSN: 15573117     Source Type: Journal    
DOI: 10.1016/j.healun.2012.01.866     Document Type: Article

References (103)

1. E.A. Pomfret, R.S. Sung, J. Allan, M. Kinkhabwala, J.K. Melancon, J.P. Roberts Solving the organ shortage crisis: the 7th annual American Society of Transplant Surgeons' State-of-the-Art Winter Symposium Am J Transplant 8 2008 745 752 (Pubitemid 351347756)
2. C. Meers, D. Van Raemdonck, G.M. Verleden The number of lung transplants can be safely doubled using extended criteria donors; a single-center review Transpl Int 23 2010 628 635
3. M. Cypel, J.C. Yeung, M. Liu Normothermic ex vivo lung perfusion in clinical lung transplantation N Engl J Med 364 2011 1431 1440
4. S. Lindstedt, J. Hlebowicz, B. Koul Comparative outcome of double lung transplantation using conventional donor lungs and non-acceptable donor lungs reconditioned ex vivo Interact Cardiovasc Thorac Surg 12 2011 162 165
5. F.J. Veith, J.W. Hagstrom, S.L. Nehlsen, R.C. Karl, M. Deysine Functional, hemodynamic, and anatomic changes in isolated perfused dog lungs: the importance of perfusate characteristics Ann Surg 165 1967 267 278
6. G. Nicolaysen Perfusate qualities and spontaneous edema formation in an isolated perfused lung preparation Acta Physiol Scand 83 1971 563 570
7. J. Czartolomna, N.F. Voelkel, S.W. Chang Permeability characteristics of isolated perfused rat lungs J Appl Physiol 70 1991 1854 1860
8. A.B. Fisher, C. Dodia, J. Linask Perfusate composition and edema formation in isolated rat lungs Exp Lung Res 1 1980 13 21 (Pubitemid 11198603)
9. S.L. Young An isolated perfused rat lung preparation Environ Health Perspect 16 1976 61 66 (Pubitemid 8037529)
10. S. Sasaki, K. Yasuda, J. LoCicero 3rd Reliable 18-hour lung preservation with University of Wisconsin solution An ex vivo rat model with a pulsatile perfusion system Nihon Kyobu Geka Gakkai Zasshi 47 1999 99 103
11. M. Cypel, J.C. Yeung, S. Hirayama Technique for prolonged normothermic ex vivo lung perfusion J Heart Lung Transplant 27 2008 1319 1325
12. F. Petak, W. Habre, Z. Hantos, P.D. Sly, D.R. Morel Effects of pulmonary vascular pressures and flow on airway and parenchymal mechanics in isolated rat lungs J Appl Physiol 92 2002 169 178 (Pubitemid 34670003)
13. A.F. Broccard, C. Vannay, F. Feihl, M.D. Schaller Impact of low pulmonary vascular pressure on ventilator-induced lung injury Crit Care Med 30 2002 2183 2190 (Pubitemid 35191565)
14. T.S. Hakim, R.P. Michel, H.K. Chang Effect of lung inflation on pulmonary vascular resistance by arterial and venous occlusion J Appl Physiol 53 1982 1110 1115 (Pubitemid 13220593)
15. J.B. West, C.T. Dollery Distribution of blood flow and ventilation-perfusion ratio in the lung, measured with radioactive carbon dioxide J Appl Physiol 15 1960 405 410
16. J.B. West Distribution of pulmonary blood flow and ventilation measured with radioactive gases Scand J Respir Dis Suppl 62 1966 9 13
17. W. Mitzner, J.T. Sylvester Lymph flow and lung weight in isolated sheep lungs J Appl Physiol 61 1986 1830 1835 (Pubitemid 17196241)
18. H.S. Goldberg, W. Mitzner, G. Batra Effect of transpulmonary and vascular pressures on rate of pulmonary edema formation J Appl Physiol 43 1977 14 19 (Pubitemid 8169322)
19. Z. Fu, M.L. Costello, K. Tsukimoto High lung volume increases stress failure in pulmonary capillaries J Appl Physiol 73 1992 123 133
20. J.C. Parker, M.I. Townsley, B. Rippe, A.E. Taylor, J. Thigpen Increased microvascular permeability in dog lungs due to high peak airway pressures J Appl Physiol 57 1984 1809 1816 (Pubitemid 15191381)
21. J. Bhattacharya, M.A. Gropper, J.M. Shepard Lung expansion and the perialveolar interstitial pressure gradient J Appl Physiol 66 1989 2600 2605 (Pubitemid 19164957)
22. G.A. Patterson, W.A. Mitzner, J.T. Sylvester Assessment of fluid balance in isolated sheep lungs J Appl Physiol 58 1985 882 891 (Pubitemid 15058817)
23. P.K. Lunde, B.A. Waaler Transvascular fluid balance in the lung J Physiol 205 1969 1 18
24. J.S. Kerr, N.J. Baker, D.J. Bassett, A.B. Fisher Effect of perfusate glucose concentration on rat lung glycolysis Am J Physiol 236 1979 E229 E233
25. R.W. Niemeier The isolated perfused lung Environ Health Perspect 56 1984 35 41 (Pubitemid 14070477)
26. R.A. Rhoades Isolated perfused lung preparation for studying altered gaseous environments Environ Health Perspect 56 1984 43 50 (Pubitemid 14070478)
27. R.S. Chang, K. Wright, R.M. Effros Role of albumin in prevention of edema in perfused rabbit lungs J Appl Physiol 50 1981 1065 1070 (Pubitemid 11107543)
28. L. Brasile, B.M. Stubenitsky, M.H. Booster, D. Arenada, C. Haisch, G. Kootstra Transfection and transgene expression in a human kidney during ex vivo warm perfusion Transplant Proc 34 2002 2624 (Pubitemid 35304858)
29. A. Hauge, P.K. Lunde, B.A. Waaler Vasoconstriction in isolated blood-perfused rabbit lungs and its inhibition by cresols Acta Physiol Scand 66 1966 226 240
30. S.A. Kraft, S. Fujishima, G.P. McGuire, J.S. Thompson, T.A. Raffin, R.G. Pearl Effect of blood and albumin on pulmonary hypertension and edema in perfused rabbit lungs J Appl Physiol 78 1995 499 504
31. D.B. Pearse, J.T. Sylvester Spontaneous injury in isolated sheep lungs: role of resident polymorphonuclear leukocytes J Appl Physiol 72 1992 2475 2481
32. F.R. Rega, E.J. Vandezande, N.C. Jannis, G.M. Verleden, T.E. Lerut, D.E. Van Raemdonck The role of leukocyte depletion in ex vivo evaluation of pulmonary grafts from (non-)heart-beating donors Perfusion 18 Suppl 1 2003 13 21 (Pubitemid 36503925)
33. R. Souilamas, J.I. Souilamas Jr, M. Saueressig, R. Briot Advanced normothermic ex vivo lung maintenance using the mobile Organ Care System J Heart Lung Transplant 30 2011 847 848
34. T. Jaecklin, D. Engelberts, G. Otulakowski, H. O'Brodovich, M. Post, B.P. Kavanagh Lung-derived soluble mediators are pathogenic in ventilator-induced lung injury Am J Physiol Lung Cell Mol Physiol 300 2011 L648 L658
35. T. Kakishita, T. Oto, S. Hori Suppression of inflammatory cytokines during ex vivo lung perfusion with an adsorbent membrane Ann Thorac Surg 89 2010 1773 1779
36. M.R. Sadaria, P.D. Smith, D.A. Fullerton Cytokine expression profile in human lungs undergoing normothermic ex-vivo lung perfusion Ann Thorac Surg 92 2011 478 484
37. C.L. Evans, F.Y. Hsu, T. Kosaka Utilization of blood sugar and formation of lactic acid by the lungs J Physiol 82 1934 41 61
38. A.B. Fisher, H. Steinberg, D. Bassett Energy utilization by the lung Am J Med 57 1974 437 446
39. S.L. Young, J.J. O'Neil, R.S. Kasuyama, D.F. Tierney Glucose utilization by edematous rat lungs Lung 157 1980 165 177 (Pubitemid 10102639)
40. D.F. Tierney, S.L. Young, J.J. O'Neil, M. Abe Isolated perfused lungsubstrate utilization Fed Proc 36 1977 161 165
41. T. Dalhamn, A. Rosengren The effect of oxygen lack on the tracheal ciliary activity Arch Environ Health 16 1968 371 373
42. D.J. Bassett, A.B. Fisher Pentose cycle activity of the isolated perfused rat lung Am J Physiol 231 1976 1527 1532
43. M. Chvapil Lactate dehydrogenase isoenzyme pattern and total LDH activity in the lung and liver of rats chronically exposed to low and high oxygen concentrations Life Sci 17 1975 762 766
44. D.J. Bassett, A.B. Fisher Stimulation of rat lung metabolism with 2,4-dinitrophenol and phenazine methosulfate Am J Physiol 231 1976 898 902
45. M. Basaran, K. Sever, E. Kafali Serum lactate level has prognostic significance after pediatric cardiac surgery J Cardiothorac Vasc Anesth 20 2006 43 47 (Pubitemid 43182775)
46. A.B. Fisher Intermediary metabolism of the lung Environ Health Perspect 55 1984 149 158 (Pubitemid 14094805)
47. T. Koike, J.C. Yeung, M. Cypel Kinetics of lactate metabolism during acellular normothermic ex vivo lung perfusion J Heart Lung Transplant 30 2011 1312 1319
48. A.B. Fisher, C. Dodia Lactate and regulation of lung glycolytic rate Am J Physiol 246 1984 E426 E429
49. F. Valenza, L. Rosso, M. Pizzocri The consumption of glucose during ex vivo lung perfusion correlates with lung edema Transplant Proc 43 2011 993 996
50. M.E. Shaw, R.A. Rhoades Substrate metabolism in the perfused lung: response to changes in circulating glucose and palmitate levels Lipids 12 1977 930 935 (Pubitemid 8230592)
51. W.J. Longmore, J.T. Mourning Lactate production in isolated perfused rat lung Am J Physiol 231 1976 351 354
52. G.D. Massaro, D.B. Gail, D. Massaro Lung oxygen consumption and mitochondria of alveolar epithelial and endothelial cells J Appl Physiol 38 1975 588 592
53. R.A. Rhoades, D.A. Ryder Fetal lung metabolism Response to maternal fasting Biochim Biophys Acta 663 1981 621 629 (Pubitemid 11159341)
54. E.M. Postlethwait, S.L. Young Alteration of rat lung adenine nucleotide content after pulmonary edema Lung 158 1980 157 164 (Pubitemid 10021275)
55. W.A. Stubbs, I. Morgan, B. Lloyd, K.G. Alberti The effect of insulin on lung metabolism in the rat Clinical Endocrinol 7 1977 181 184 (Pubitemid 8251271)
56. S. Steen, Q. Liao, P.N. Wierup, R. Bolys, L. Pierre, T. Sjoberg Transplantation of lungs from non-heart-beating donors after functional assessment ex vivo Ann Thorac Surg 76 2003 244 252 discussion 52 (Pubitemid 36819750)
57. M. Cypel, M. Rubacha, J. Yeung Normothermic ex vivo perfusion prevents lung injury compared to extended cold preservation for transplantation Am J Transplant 9 2009 2262 2269
58. R.J. Mason, M.C. Williams, J.H. Widdicombe Fluid and electrolyte transport across monolayers of alveolar type II cells in vitro Am Rev Respir Dis 127 1983 S24 S28
59. A.P. Comellas, A.M. Kelly, H.E. Trejo Insulin regulates alveolar epithelial function by inducing Na+/K+-ATPase translocation to the plasma membrane in a process mediated by the action of Akt J Cell Sci 123 2010 1343 1351
60. J.D. Aitchison, H.E. Orr, P.A. Flecknell, J.A. Kirby, J.H. Dark Functional assessment of non-heart-beating donor lungs: prediction of post-transplant function Eur J Cardiothorac Surg 20 2001 187 194 (Pubitemid 32567589)
61. J.C. Yeung, T. Koike, M. Cypel Airway pressure and compliance in the evaluation of donor lung injury during protective ex vivo lung perfusion in a porcine brain death model [abstract 420] J Heart Lung Transplant 30 2011 S143
62. P.G. Sanchez, G.J. Bittle, H.S. Son Ex-vivo perfusion reduces lung lipid peroxidation in a swine model of cardiac death [abstract 423] J Heart and Lung Transplantation 30 2011 S144
63. S. Wipper, A. Lueke, S. Baldus, J. Schirmer, H. Reichenspurner, F.M. Wagner Myeloperoxidase tissue level (mpo) reflects successful repair of donor lung injury by ex-vivo lung perfusion (EVLP) [abstract 421] J Heart Lung Transplant 30 2011 S143S4
64. R. Briot, J.A. Frank, T. Uchida, J.W. Lee, C.S. Calfee, M.A. Matthay Elevated levels of the receptor for advanced glycation end products, a marker of alveolar epithelial type I cell injury, predict impaired alveolar fluid clearance in isolated perfused human lungs Chest 135 2009 269 275
65. S.E. Verleden, R. Vos, V. Mertens Heterogeneity of chronic lung allograft dysfunction: insights from protein expression in broncho alveolar lavage J Heart Lung Transplant 30 2011 667 673
66. P. Wierup, A. Haraldsson, F. Nilsson Ex vivo evaluation of nonacceptable donor lungs Ann Thorac Surg 81 2006 460 466 (Pubitemid 43120535)
67. T.M. Egan, J.A. Haithcock, W.A. Nicotra Ex vivo evaluation of human lungs for transplant suitability Ann Thorac Surg 81 2006 1205 1213
68. I. Inci, W. Zhai, S. Arni Fibrinolytic treatment improves the quality of lungs retrieved from non-heart-beating donors J Heart Lung Transplant 26 2007 1054 1060 (Pubitemid 47494662)
69. B.M. Dong, J.B. Abano, T.M. Egan Nitric oxide ventilation of rat lungs from non-heart-beating donors improves posttransplant function Am J Transplant 9 2009 2707 2715
70. B. Dong, T. Egan Post-mortem and ex-vivo carbon monoxide (CO) ventilation reduces ischemia-reperfusion injury (IRI) in rat lungs transplanted from non-heart-beating donors (NHBDs) [abstract 280] J Heart Lung Transplant 29 2010 S95
71. I. Inci, L. Ampollini, S. Arni Ex vivo reconditioning of marginal donor lungs injured by acid aspiration J Heart Lung Transplant 27 2008 1229 1236
72. C.M. Meers, S. Wauters, E. Verbeken Preemptive therapy with steroids but not macrolides improves gas exchange in caustic-injured donor lungs J Surg Res 170 2011 e141 e148
73. C. Van de Wauwer, A.P. Neyrinck, N. Geudens The mode of death in the non-heart-beating donor has an impact on lung graft quality Eur J Cardiothorac Surg 36 2009 919 926
74. F.R. Rega, N.C. Jannis, G.M. Verleden, T.E. Lerut, D.E. Van Raemdonck Long-term preservation with interim evaluation of lungs from a non-heart-beating donor after a warm ischemic interval of 90 minutes Ann Surg 238 2003 782 792 discussion 92-3
75. C. Van De Wauwer, A.P. Neyrinck, N. Geudens Retrograde flush following warm ischemia in the non-heart-beating donor results in superior graft performance at reperfusion J Surg Res 154 2009 118 125
76. M.E. Erasmus, M.H. Fernhout, J.M. Elstrodt, G. Rakhorst Normothermic ex vivo lung perfusion of non-heart-beating donor lungs in pigs: from pretransplant function analysis towards a 6-h machine preservation Transplant Int 19 2006 589 593 (Pubitemid 43881759)
77. D. Nakajima, T. Yamada, F. Chen Reconditioning of lungs from non-heart-beating donors with normothermic ex vivo lung perfusion [abstract 91] J Heart Lung Transplant 30 2011 S38 S39
78. T. Yamada, D. Nakajima, J. Sakamoto 422 Reconditioning of Lungs with Pulmonary Edema in Ex vivo Lung Perfusion Circuit J Heart Lung Transplant 30 2011 S144
79. D.M. Karamanou, J. Perry, H.R. Walden The effect of ex-vivo perfusion on the microbiological profile of the donor lung [abstract 279] J Heart Lung Transplant 29 2010 S94
80. J.C. Yeung, D. Wagnetz, M. Cypel Ex vivo adenoviral mediated IL-10 gene therapy (AdhIL-10) improves lung function with a reduced vector associated inflammatory response [abstract 170] J Heart Lung Transplant 28 2009 S125
81. I.L. Medeiros, P.M. Pêgo-Fernandes, A.W. Mariani et al. Histologic and functional evaluation of lungs reconditioned by ex vivo lung perfusion J Heart Lung Transplant 2011 [Epub ahead of print: http://dx.doi.org/10.1016/j. healun.2011.10.005 ]
82. S. Otani, T. Oto, T. Kakishita Early effects of the ex vivo evaluation system on graft function after swine lung transplantation Eur J Cardiothorac Surg 40 2011 956 961
83. S. Lindstedt, A. Eyjolfsson, B. Koul How to recondition ex vivo initially rejected donor lungs for clinical transplantation: clinical experience from Lund university hospital J Transplant 2011 2011 754383
84. A.F. Pierre, K.N. DeCampos, M. Liu Rapid reperfusion causes stress failure in ischemic rat lungs J Thorac Cardiovasc Surg 116 1998 932 942 (Pubitemid 28553535)
85. G.R. Barer, J.W. Shaw Pulmonary vasodilator and vasoconstrictor actions of carbon dioxide J Physiol 213 1971 633 645
86. C. Aigner, A. Slama, K. Htzenecker Clinical ex vivo lung perfusionpushing the limits [abstract 88] J Heart Lung Transplant 30 2011 S38
87. F.J. Moradiellos, J.M. Naranjo, M. Crdoba Clinical lung transplantation after ex vivo evaluation of uncontrolled non heart-beating donors lungs: initial experience [abstract 90] J Heart Lung Transplant 30 2011 S38
88. B. Zych, A.F. Popov, G. Stavri et al. Early outcomes of bilateral sequential single lung transplantation after ex-vivo lung evaluation and reconditioning J Heart Lung Transplant 2011 [Epub ahead of print: http://dx.doi.org/10.1016/j.healun.2011.10.008 ]
89. R. Ingemansson, A. Eyjolfsson, L. Mared Clinical transplantation of initially rejected donor lungs after reconditioning ex vivo Ann Thorac Surg 87 2009 255 260
90. J.A. Frank, R. Briot, J.W. Lee, A. Ishizaka, T. Uchida, M.A. Matthay Physiological and biochemical markers of alveolar epithelial barrier dysfunction in perfused human lungs Am J Physiol Lung Cell Mol Physiol 293 2007 L52 L59
91. J.W. Lee, X. Fang, N. Gupta, V. Serikov, M.A. Matthay Allogeneic human mesenchymal stem cells for treatment of E. coli endotoxin-induced acute lung injury in the ex vivo perfused human lung Proc Natl Acad Sci U S A 106 2009 16357 16362
92. M. Krampera Mesenchymal stromal cells: more than inhibitory cells Leukemia 25 2011 565 566
93. A. Krasnodembskaya, Y. Song, X. Fang Antibacterial effect of human mesenchymal stem cells is mediated in part from secretion of the antimicrobial peptide LL-37 Stem Cells 28 2010 2229 2238
94. S. Aggarwal, M.F. Pittenger Human mesenchymal stem cells modulate allogeneic immune cell responses Blood 105 2005 1815 1822 (Pubitemid 40223708)
95. H. Kanazawa, Y. Fujimoto, T. Teratani Bone marrow-derived mesenchymal stem cells ameliorate hepatic ischemia reperfusion injury in a rat model PloS One 6 2011 e19195
96. C. Lange, F. Togel, H. Ittrich Administered mesenchymal stem cells enhance recovery from ischemia/reperfusion-induced acute renal failure in rats Kidney Int 68 2005 1613 1617 (Pubitemid 43169906)
97. M. Cypel, M. Liu, M. Rubacha Functional repair of human donor lungs by IL-10 gene therapy Sci Transl Med 1 2009 4ra9
98. A. Emaminia, D.J. Lapar, Y. Zhao Adenosine A(2A) agonist improves lung function during ex vivo lung perfusion Ann Thorac Surg 92 2011 1840 1846
99. H.C. Ott, B. Clippinger, C. Conrad Regeneration and orthotopic transplantation of a bioartificial lung Nat Med 16 2010 927 933
100. T.H. Petersen, E.A. Calle, M.B. Colehour, L.E. Niklason Matrix Composition and Mechanics of Decellularized Lung Scaffolds Cells Tissues Organs 2011 [Epub ahead of print: doi: 10.1159/000324896 ]
101. J.J. Song, S.S. Kim, Z. Liu Enhanced in vivo function of bioartificial lungs in rats Ann Thorac Surg 92 2011 998 1005 discussion 1006
102. G. Singh, J. Javidfar, J. Costa Perfusion/decellularization of large animal lungs [abstract 549] J Heart Lung Transplant 30 2011 S184 S185
103. J.J. Song, H.C. Ott Bioartificial lung engineering Am J Transplant 12 2012 283 288