Progress of Clinical Application for Ex Vivo Lung Perfusion in Lung Transplantation_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

GUChang ¹ , YEBo ¹ , SUNYi-feng ¹ , LIXin ² ,  ZHAOHeng ¹ ,  GAOWen ^1,3

1. Department of Thoracic Surgery, Shanghai Chest Hospital, Shanghai Jiaotong University, Shanghai 200030, P. R. China;
2. Department of Cardiopulmonary Bypass, Shanghai Chest Hospital, Shanghai Jiaotong University, Shanghai 200030, P. R. China;
3. Department of Thoracic Surgery, Huadong Hospital, Fudan University, Shanghai 200040, P. R. China;

Corresponding author：

ZHAOHeng, Email: h_zhao-28@163.com; GAOWen, Email: gaowen5921@163.com

Keywords：

Ex vivo lung perfusion; Lung transplantation; Lung function

DOI：

10.7507/1007-4848.20160258

Video：

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Lung transplantation has been a standard treatment option for patients with end-stage lung disease. However, the demand for donor lungs exceeds the poor of available organs, resulting in considerable waiting list mortality. Among all the useful methods so far, ex vivo lung perfusion (EVLP) has been considered a useful technique in lung transplantation, which helps prolong donor lung preservation and repair donor lung injuries. Current studies have demonstrated EVLP can evaluate the donor lung function continuously and provide platform for pharmaceutical or even gene therapy. Moreover, EVLP improves the function of marginal donor lungs and increases the quantity of lungs meeting the transplant criteria, which could extend the donor pool. This article reviews the clinical application and research progress of EVLP in lung transplantation.

Citation： GUChang, YEBo, SUNYi-feng, LIXin, ZHAOHeng, GAOWen. Progress of Clinical Application for Ex Vivo Lung Perfusion in Lung Transplantation. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2016, 23(11): 1103-1107. doi: 10.7507/1007-4848.20160258 Copy

1.	Lund LH, Edwards LB, Kucheryavaya AY, et al. The registry of the international society for heart and lung transplantation: thirty-second official adult heart transplantation report-2015; focus theme: Early graft failure. J Heart Lung Transplant, 2015, 34(10): 1244.
2.	Pierre AF, Sekine Y, Hutcheon MA, et al. Marginal donor lungs: a reassessment. J Thorac Cardiovasc Surg, 2002, 123(3): 421-428.
3.	Egan TM, Haithcock JA, Nicotra WA, et al. Ex vivo evaluation of human lungs for transplant suitability. Ann Thorac Surg, 2006, 81(4): 1205-1213.
4.	Ingemansson R, Eyjolfsson A, Mared L, et al. Clinical transplanta-tion of initially rejected donor lungs after reconditioning ex vivo. Ann Thorac Surg, 2009, 87(1): 255-260.
5.	Aigner C, Slama A, Hötzenecker K, et al. Clinical ex vivo lung perfusion-pushing the limits. Am J Transplant, 2012, 12(7): 1839-1847.
6.	Yusen RD. Lung transplantation outcomes: the importance and inadequacies of assessing survival. Am J Transplant, 2009, 9(7): 1493-1494.
7.	Schiavon M, Falcoz PE, Santelmo N, et al. Does the use of extended criteria donors influence early and long-term results of lung transp-lantation? Interact Cardiovasc Thorac Surg, 2012, 14(2): 183-187.
8.	Sommer W, Kühn C, Tudorache I, et al. Extended criteria donor lungs and clinical outcome: results of an alternative allocation algorithm. J Heart Lung Transplant, 2013, 32(11): 1065-1072.
9.	Cypel M, Sato M, Yildirim E, et al. Initial experience with lung donation after cardiocirculatory death in Canada. J Heart Lung Transplant, 2009, 28(8): 753-758.
10.	Levvey BJ, Harkess M, Hopkins P, et al. Excellent clinical outcomes from a national donation‐after‐determination‐of‐cardiac‐death lung transplant collaborative. Am J Transplant, 2012, 12(9): 2406-2413.
11.	de Antonio DG, Marcos R, Laporta R, et al. Results of clinical lung transplant from uncontrolled non-heart-beating donors. J Heart Lung Transplant, 2007, 26(5): 529-534.
12.	Bonser RS, Taylor R, Collett D, et al. Effect of donor smoking on survival after lung transplantation: a cohort study of a prospective registry. Lancet, 2012, 380(9843): 747-755.
13.	Sabashnikov A, Patil NP, Mohite PN, et al. Influence of donor smoking on midterm outcomes after lung transplantation. Ann Thorac Surg, 2014, 97(3): 1015-1021.
14.	Carrel A, Lindbergh CA. The culture of whole organs. Science, 1935, 81(2112): 621-623.
15.	Steen S, Sjöberg T, Pierre L, et al. Transplantation of lungs from a non-heart-beating donor. Lancet, 2001, 357(9259): 825-829.
16.	Cypel M, Yeung JC, Hirayama S, et al. Technique for prolonged normothermic ex vivo lung perfusion. J Heart Lung Transplant, 2008, 27(12): 1319-1325.
17.	Cypel M, Yeung JC, Liu M, et al. Normothermic ex vivo lung perfu-sion in clinical lung transplantation. N Engl J Med, 2011, 364(15): 1431-1440.
18.	Cypel M, Keshavjee S. Extracorporeal lung perfusion. Curr Opin Organ Transplant, 2011, 16(5): 469-475.
19.	Fischer S, Matte-Martyn A, de Perrot M, et al. Low-potassium dextran preservation solution improves lung function after human lung transplantation. J Thorac Cardiovasc Surg, 2001, 121(3): 594-596.
20.	Steen S, Liao Q, Wierup PN, et al. Transplantation of lungs from non–heart-beating donors after functional assessment ex vivo. Ann Thorac Surg, 2003, 76(1): 244-252.
21.	Díez FJM, de Ugarte AV. Ex-vivo perfusion: assessment, recovery and optimisation of human lungs for transplant. Arch Broncone-umol, 2010, 46(5): 213-214.
22.	Oka T, Puskas JD, Mayer E, et al. Low-potassium UW solution for lung preservation: comparison with regular UW, LPD, and Euro-Collins solutions. Transplantation, 1991, 52(6): 984-988.
23.	Inci I, Ampollini L, Arni S, et al. Ex vivo reconditioning of marginal donor lungs injured by acid aspiration. J Heart Lung Transplant, 2008, 27(11): 1229-1236.
24.	Andrade CF, Martins LK, Tonietto TA, et al. Partial liquid ventila-tion with perfluorodecalin following unilateral canine lung allotran-splantation in non–heart-heating donors. J Heart Lung Transplant, 2004, 23(2): 242-251.
25.	Valenza F, Rosso L, Pizzocri M, et al. The consumption of glucose during ex vivo lung perfusion correlates with lung edema. Trans-plant Proc, 2011, 43(4): 993-996.
26.	Meers CM, Tsagkaropoulos S, Wauters S, et al. A model of ex vivo perfusion of porcine donor lungs injured by gastric aspiration: a step towards pretransplant reconditioning. J Surg Res, 2011, 170(1): 159-167.
27.	Medeiros IL, Pêgo-Fernandes PM, Mariani AW, et al. Histologic and functional evaluation of lungs reconditioned by ex vivo lung perfusion. J Heart Lung Transplant, 2012, 31(3): 305-309.
28.	De Perrot M, Sekine Y, Fischer S, et al. Interleukin-8 release during early reperfusion predicts graft function in human lung transplanta-tion. Am J Respir Crit Care Med, 2002, 165(2): 211-215.
29.	Sadaria MR, Smith PD, Fullerton DA, et al. Cytokine expression profile in human lungs undergoing normothermic ex-vivo lung perfusion. Ann Thorac Surg, 2011, 92(2): 478-484.
30.	Ware LB, Wang Y, Fang X, et al. Assessment of lungs rejected for transplantation and implications for donor selection. Lancet, 2002, 360(9333): 619-620.
31.	Inci I, Zhai W, Arni S, et al. Fibrinolytic treatment improves the quality of lungs retrieved from non-heart-beating donors. J Heart Lung Transplant, 2007, 26(10): 1054-1060.
32.	Inci I, Yamada Y, Hillinger S, et al. Successful lung transplantation after donor lung reconditioning with urokinase in ex vivo lung perfusion system. Ann Thorac Surg, 2014, 98(5): 1837-1838.
33.	Andreasson A, Karamanou DM, Perry JD, et al. The effect of ex vivo lung perfusion on microbial load in human donor lungs. J Heart Lung Transplant, 2014, 33(9): 910-916.
34.	Nakajima D, Cypel M, Bonato R, et al. Ex vivo perfusion treatment of infection in human donor lungs. Am J Transplant, 2016, 16(4): 1229-1237.
35.	Kondo T, Chen F, Ohsumi A, et al. β 2-adrenoreceptor agonist inhalation during ex vivo lung perfusion attenuates lung injury. Ann Thorac Surg, 2015, 100(2): 480-486.
36.	Noda K, Shigemura N, Tanaka Y, et al. Hydrogen preconditioning during ex vivo lung perfusion improves the quality of lung grafts in rats. Transplantation, 2014, 98(5): 499-506.
37.	Harada M, Oto T, Otani S, et al. A neutrophil elastase inhibitor improves lung function during ex vivo lung perfusion. Gen Thorac Cardiovasc Surg, 2015, 18(9): 1-7.
38.	Cypel M, Liu M, Rubacha M, et al. Functional repair of human donor lungs by IL-10 gene therapy. Sci Transl Med, 2009, 1(4): 1-9.
39.	Lee JW, Fang X, Gupta N, et al. Allogeneic human mesenchymal stem cells for treatment of E. coli endotoxin-induced acute lung injury in the ex vivo perfused human lung. Proc Nati Acad Sci USA, 2009, 106(38): 16357-16362.
40.	Valenza F, Rosso L, Coppola S, et al. Ex vivo lung perfusion to improve donor lung function and increase the number of organs available for transplantation. Transpl Int, 2014, 27(6): 553-561.

1. Lund LH, Edwards LB, Kucheryavaya AY, et al. The registry of the international society for heart and lung transplantation: thirty-second official adult heart transplantation report-2015; focus theme: Early graft failure. J Heart Lung Transplant, 2015, 34(10): 1244.
2. Pierre AF, Sekine Y, Hutcheon MA, et al. Marginal donor lungs: a reassessment. J Thorac Cardiovasc Surg, 2002, 123(3): 421-428.
3. Egan TM, Haithcock JA, Nicotra WA, et al. Ex vivo evaluation of human lungs for transplant suitability. Ann Thorac Surg, 2006, 81(4): 1205-1213.
4. Ingemansson R, Eyjolfsson A, Mared L, et al. Clinical transplanta-tion of initially rejected donor lungs after reconditioning ex vivo. Ann Thorac Surg, 2009, 87(1): 255-260.
5. Aigner C, Slama A, Hötzenecker K, et al. Clinical ex vivo lung perfusion-pushing the limits. Am J Transplant, 2012, 12(7): 1839-1847.
6. Yusen RD. Lung transplantation outcomes: the importance and inadequacies of assessing survival. Am J Transplant, 2009, 9(7): 1493-1494.
7. Schiavon M, Falcoz PE, Santelmo N, et al. Does the use of extended criteria donors influence early and long-term results of lung transp-lantation? Interact Cardiovasc Thorac Surg, 2012, 14(2): 183-187.
8. Sommer W, Kühn C, Tudorache I, et al. Extended criteria donor lungs and clinical outcome: results of an alternative allocation algorithm. J Heart Lung Transplant, 2013, 32(11): 1065-1072.
9. Cypel M, Sato M, Yildirim E, et al. Initial experience with lung donation after cardiocirculatory death in Canada. J Heart Lung Transplant, 2009, 28(8): 753-758.
10. Levvey BJ, Harkess M, Hopkins P, et al. Excellent clinical outcomes from a national donation‐after‐determination‐of‐cardiac‐death lung transplant collaborative. Am J Transplant, 2012, 12(9): 2406-2413.
11. de Antonio DG, Marcos R, Laporta R, et al. Results of clinical lung transplant from uncontrolled non-heart-beating donors. J Heart Lung Transplant, 2007, 26(5): 529-534.
12. Bonser RS, Taylor R, Collett D, et al. Effect of donor smoking on survival after lung transplantation: a cohort study of a prospective registry. Lancet, 2012, 380(9843): 747-755.
13. Sabashnikov A, Patil NP, Mohite PN, et al. Influence of donor smoking on midterm outcomes after lung transplantation. Ann Thorac Surg, 2014, 97(3): 1015-1021.
14. Carrel A, Lindbergh CA. The culture of whole organs. Science, 1935, 81(2112): 621-623.
15. Steen S, Sjöberg T, Pierre L, et al. Transplantation of lungs from a non-heart-beating donor. Lancet, 2001, 357(9259): 825-829.
16. Cypel M, Yeung JC, Hirayama S, et al. Technique for prolonged normothermic ex vivo lung perfusion. J Heart Lung Transplant, 2008, 27(12): 1319-1325.
17. Cypel M, Yeung JC, Liu M, et al. Normothermic ex vivo lung perfu-sion in clinical lung transplantation. N Engl J Med, 2011, 364(15): 1431-1440.
18. Cypel M, Keshavjee S. Extracorporeal lung perfusion. Curr Opin Organ Transplant, 2011, 16(5): 469-475.
19. Fischer S, Matte-Martyn A, de Perrot M, et al. Low-potassium dextran preservation solution improves lung function after human lung transplantation. J Thorac Cardiovasc Surg, 2001, 121(3): 594-596.
20. Steen S, Liao Q, Wierup PN, et al. Transplantation of lungs from non–heart-beating donors after functional assessment ex vivo. Ann Thorac Surg, 2003, 76(1): 244-252.
21. Díez FJM, de Ugarte AV. Ex-vivo perfusion: assessment, recovery and optimisation of human lungs for transplant. Arch Broncone-umol, 2010, 46(5): 213-214.
22. Oka T, Puskas JD, Mayer E, et al. Low-potassium UW solution for lung preservation: comparison with regular UW, LPD, and Euro-Collins solutions. Transplantation, 1991, 52(6): 984-988.
23. Inci I, Ampollini L, Arni S, et al. Ex vivo reconditioning of marginal donor lungs injured by acid aspiration. J Heart Lung Transplant, 2008, 27(11): 1229-1236.
24. Andrade CF, Martins LK, Tonietto TA, et al. Partial liquid ventila-tion with perfluorodecalin following unilateral canine lung allotran-splantation in non–heart-heating donors. J Heart Lung Transplant, 2004, 23(2): 242-251.
25. Valenza F, Rosso L, Pizzocri M, et al. The consumption of glucose during ex vivo lung perfusion correlates with lung edema. Trans-plant Proc, 2011, 43(4): 993-996.
26. Meers CM, Tsagkaropoulos S, Wauters S, et al. A model of ex vivo perfusion of porcine donor lungs injured by gastric aspiration: a step towards pretransplant reconditioning. J Surg Res, 2011, 170(1): 159-167.
27. Medeiros IL, Pêgo-Fernandes PM, Mariani AW, et al. Histologic and functional evaluation of lungs reconditioned by ex vivo lung perfusion. J Heart Lung Transplant, 2012, 31(3): 305-309.
28. De Perrot M, Sekine Y, Fischer S, et al. Interleukin-8 release during early reperfusion predicts graft function in human lung transplanta-tion. Am J Respir Crit Care Med, 2002, 165(2): 211-215.
29. Sadaria MR, Smith PD, Fullerton DA, et al. Cytokine expression profile in human lungs undergoing normothermic ex-vivo lung perfusion. Ann Thorac Surg, 2011, 92(2): 478-484.
30. Ware LB, Wang Y, Fang X, et al. Assessment of lungs rejected for transplantation and implications for donor selection. Lancet, 2002, 360(9333): 619-620.
31. Inci I, Zhai W, Arni S, et al. Fibrinolytic treatment improves the quality of lungs retrieved from non-heart-beating donors. J Heart Lung Transplant, 2007, 26(10): 1054-1060.
32. Inci I, Yamada Y, Hillinger S, et al. Successful lung transplantation after donor lung reconditioning with urokinase in ex vivo lung perfusion system. Ann Thorac Surg, 2014, 98(5): 1837-1838.
33. Andreasson A, Karamanou DM, Perry JD, et al. The effect of ex vivo lung perfusion on microbial load in human donor lungs. J Heart Lung Transplant, 2014, 33(9): 910-916.
34. Nakajima D, Cypel M, Bonato R, et al. Ex vivo perfusion treatment of infection in human donor lungs. Am J Transplant, 2016, 16(4): 1229-1237.
35. Kondo T, Chen F, Ohsumi A, et al. β 2-adrenoreceptor agonist inhalation during ex vivo lung perfusion attenuates lung injury. Ann Thorac Surg, 2015, 100(2): 480-486.
36. Noda K, Shigemura N, Tanaka Y, et al. Hydrogen preconditioning during ex vivo lung perfusion improves the quality of lung grafts in rats. Transplantation, 2014, 98(5): 499-506.
37. Harada M, Oto T, Otani S, et al. A neutrophil elastase inhibitor improves lung function during ex vivo lung perfusion. Gen Thorac Cardiovasc Surg, 2015, 18(9): 1-7.
38. Cypel M, Liu M, Rubacha M, et al. Functional repair of human donor lungs by IL-10 gene therapy. Sci Transl Med, 2009, 1(4): 1-9.
39. Lee JW, Fang X, Gupta N, et al. Allogeneic human mesenchymal stem cells for treatment of E. coli endotoxin-induced acute lung injury in the ex vivo perfused human lung. Proc Nati Acad Sci USA, 2009, 106(38): 16357-16362.
40. Valenza F, Rosso L, Coppola S, et al. Ex vivo lung perfusion to improve donor lung function and increase the number of organs available for transplantation. Transpl Int, 2014, 27(6): 553-561.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Progress of Clinical Application for Ex Vivo Lung Perfusion in Lung Transplantation

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