PDF herunterladen
CC BY 4.0 · Semin Liver Dis 2024; 44(03): 369-382
DOI: 10.1055/s-0044-1788674
Review Article

Combined Organ Transplantation in Patients with Advanced Liver Disease

Ingrid Wei Zhang
1   Department of Hepatology and Gastroenterology, Charité Universitätsmedizin Berlin, Berlin, Germany
2   Berlin Institute of Health (BIH) at Charité - Universitätsmedizin, Berlin, Germany
3   European Foundation for the Study of Chronic Liver Failure (EF CLIF) and Grifols Chair, Barcelona, Spain
,
Isabella Lurje
1   Department of Hepatology and Gastroenterology, Charité Universitätsmedizin Berlin, Berlin, Germany
,
Georg Lurje
4   Department of Surgery, Charité Universitätsmedizin Berlin, Berlin, Germany
,
Christoph Knosalla
5   Department of Cardiothoracic and Vascular Surgery, Deutsches Herzzentrum der Charité, Berlin, Germany
6   Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany
7   DZHK (German Centre for Cardiovascular Research), Partner Site Berlin, Berlin, Germany
,
Felix Schoenrath
5   Department of Cardiothoracic and Vascular Surgery, Deutsches Herzzentrum der Charité, Berlin, Germany
6   Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany
7   DZHK (German Centre for Cardiovascular Research), Partner Site Berlin, Berlin, Germany
,
Frank Tacke
1   Department of Hepatology and Gastroenterology, Charité Universitätsmedizin Berlin, Berlin, Germany
,
Cornelius Engelmann
1   Department of Hepatology and Gastroenterology, Charité Universitätsmedizin Berlin, Berlin, Germany
2   Berlin Institute of Health (BIH) at Charité - Universitätsmedizin, Berlin, Germany
› Institutsangaben Funding I.W.Z. is supported by the BIH Charité Clinician Scientist Program funded by the Charité – Universitätsmedizin Berlin and the Berlin Institute of Health at Charité (BIH).
› Weitere Informationen
   Lizenzen und Reprints


Abstract

Transplantation of the liver in combination with other organs is an increasingly performed procedure. Over the years, continuous improvement in survival could be realized through careful patient selection and refined organ preservation techniques, in spite of the challenges posed by aging recipients and donors, as well as the increased use of steatotic liver grafts. Herein, we revisit the epidemiology, allocation policies in different transplant zones, indications, and outcomes with regard to simultaneous organ transplants involving the liver, that is combined heart–liver, liver–lung, liver–kidney, and multivisceral transplantation. We address challenges surrounding combined organ transplantation such as equity, utility, and logistics of dual organ implantation, but also advantages that come along with combined transplantation, thereby focusing on molecular mechanisms underlying immunoprotection provided by the liver to the other allografts. In addition, the current standing and knowledge of machine perfusion in combined organ transplantation, mostly based on center experience, will be reviewed. Notwithstanding all the technical advances, shortage of organs, and the lack of universal eligibility criteria for certain multi-organ combinations are hurdles that need to be tackled in the future.

Keywords

liver transplantation - combined transplantation - allocation - immunotolerance - machine perfusion


Publikationsverlauf

Artikel online veröffentlicht:
25. Juli 2024

© 2024. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 

  • References

  • 1 Wolf JH, Sulewski ME, Cassuto JR. et al. Simultaneous thoracic and abdominal transplantation: can we justify two organs for one recipient?. Am J Transplant 2013; 13 (07) 1806-1816
    CrossrefPubMedSuche in Google Scholar
  • 2 Wilk AR, Booker SE, Stewart DE. et al. Developing simultaneous liver-kidney transplant medical eligibility criteria while providing a safety net: a 2-year review of the OPTN's allocation policy. Am J Transplant 2021; 21 (11) 3593-3607
    CrossrefPubMedSuche in Google Scholar
  • 3 Wiseman AC. Simultaneous liver-kidney transplant: long-term management (steroid withdrawal and safety net patients). Clin Liver Dis (Hoboken) 2019; 13 (06) 176-179
    CrossrefPubMedSuche in Google Scholar
  • 4 Jochmans I, van Rosmalen M, Pirenne J, Samuel U. Adult liver allocation in eurotransplant. Transplantation 2017; 101 (07) 1542-1550
    CrossrefPubMedSuche in Google Scholar
  • 5 Eurotransplant. Liver Allocation System (ELAS), version 6.5, October 2022, of the Eurotransplant Manual. Available at: https://www.eurotransplant.org/wp-content/uploads/2024/04/H5-ELAS-MELD-April-2024.pdf
    PubMed
  • 6 Eurotransplant. Allocation General, version 4.2, January 2022, of the Eurotransplant Manual. https://www.eurotransplant.org/wp-content/uploads/2022/02/H3-Allocation-v-4.2-January-2022.pdf
    PubMed
  • 7 Organ Procurement and Transplantation Network. Policies. Updated on 19 March 2024 . Accessed 11 July 2024 at: https://optn.transplant.hrsa.gov/media/eavh5bf3/optn_policies.pdf
    PubMedSuche in Google Scholar
  • 8 Westphal SG, Langewisch ED, Robinson AM. et al. The impact of multi-organ transplant allocation priority on waitlisted kidney transplant candidates. Am J Transplant 2021; 21 (06) 2161-2174
    CrossrefPubMedSuche in Google Scholar
  • 9 Westphal SG, Langewisch ED, Miles CD. Current state of multiorgan transplantation and implications for future practice and policy. Adv Chronic Kidney Dis 2021; 28 (06) 561-569
    CrossrefPubMedSuche in Google Scholar
  • 10 Eurotransplant. Kidney (ETKAS and ASP), version 2024.1, January 2024, of the Eurotransplant Manual. Available at: https://www.eurotransplant.org/wp-content/uploads/2024/01/H4-Kidney-2024.1-January-2024.pdf
    PubMed
  • 11 Cannon RM, Goldberg DS, Eckhoff DE, Anderson DJ, Orandi BJ, Locke JE. Early outcomes with the liver-kidney safety net. Transplantation 2021; 105 (06) 1261-1272
    CrossrefPubMedSuche in Google Scholar
  • 12 Engen RM, Kirmani S. Pediatric impacts of multiorgan transplant allocation policy in the United States. Pediatr Transplant 2023; 27 (Suppl. 01) e14253
    CrossrefPubMedSuche in Google Scholar
  • 13 Ivanics T, Vianna R, Kubal CA. et al. Impact of the acuity circle model for liver allocation on multivisceral transplant candidates. Am J Transplant 2022; 22 (02) 464-473
    CrossrefPubMedSuche in Google Scholar
  • 14 Starzl TE, Bilheimer DW, Bahnson HT. et al. Heart-liver transplantation in a patient with familial hypercholesterolaemia. Lancet 1984; 1 (8391) 1382-1383
    CrossrefPubMedSuche in Google Scholar
  • 15 Tracy KM, Matsuoka LK, Alexopoulos SP. Update on combined heart and liver transplantation: evolving patient selection, improving outcomes, and outstanding questions. Curr Opin Organ Transplant 2023; 28 (02) 104-109
    CrossrefPubMedSuche in Google Scholar
  • 16 Marelli AJ, Ionescu-Ittu R, Mackie AS, Guo L, Dendukuri N, Kaouache M. Lifetime prevalence of congenital heart disease in the general population from 2000 to 2010. Circulation 2014; 130 (09) 749-756
    CrossrefPubMedSuche in Google Scholar
  • 17 Kittleson MM, Sharma K, Brennan DC. et al; American Heart Association Heart Failure and Transplantation Committee of the Council on Clinical Cardiology; Council on the Kidney in Cardiovascular Disease; Council on Cardiovascular Surgery and Anesthesia; Council on Cardiovascular and Stroke Nursing; Council on Quality of Care and Outcomes Research; and Council on Lifelong Congenital Heart Disease and Heart Health in the Young. Dual-organ transplantation: indications, evaluation, and outcomes for heart-kidney and heart-liver transplantation: a scientific statement from the American Heart Association. Circulation 2023; 148 (07) 622-636
    CrossrefPubMedSuche in Google Scholar
  • 18 Taner T, Hilscher MB, Broda CR, Drenth JPH. Issues in multi-organ transplantation of the liver with kidney or heart in polycystic liver-kidney disease or congenital heart disease: current practices and immunological aspects. J Hepatol 2023; 78 (06) 1157-1168
    CrossrefPubMedSuche in Google Scholar
  • 19 Deo SV, Al-Kindi SG, Altarabsheh SE. et al. Model for end-stage liver disease excluding international normalized ratio (MELD-XI) score predicts heart transplant outcomes: evidence from the registry of the United Network for Organ Sharing. J Heart Lung Transplant 2016; 35 (02) 222-227
    CrossrefPubMedSuche in Google Scholar
  • 20 Briasoulis A, Akintoye E, Kuno T, Alvarez P. Characteristics and outcomes of patients undergoing combined organ transplantation (from the United Network for Organ Sharing). Am J Cardiol 2020; 129: 42-45
    CrossrefPubMedSuche in Google Scholar
  • 21 Bryant III R, Rizwan R, Zafar F. et al. Contemporary outcomes of combined heart-liver transplant in patients with congenital heart disease. Transplantation 2018; 102 (02) e67-e73
    CrossrefPubMedSuche in Google Scholar
  • 22 Cotter TG, Wang J, Peeraphatdit T. et al. Simultaneous heart-liver transplantation for congenital heart disease in the United States: rapidly increasing with acceptable outcomes. Hepatology 2021; 73 (04) 1464-1477
    CrossrefPubMedSuche in Google Scholar
  • 23 Atluri P, Gaffey A, Howard J. et al. Combined heart and liver transplantation can be safely performed with excellent short- and long-term results. Ann Thorac Surg 2014; 98 (03) 858-862
    CrossrefPubMedSuche in Google Scholar
  • 24 Brozzi NA, Loebe M, Souki FG. et al. En-bloc simultaneous heart-liver transplantation in adult patients. Ann Surg 2021; 274 (06) e1284-e1289
    CrossrefPubMedSuche in Google Scholar
  • 25 Barbara DW, Rehfeldt KH, Heimbach JK. et al. Perioperative management of patients undergoing combined heart-liver transplantation. Transplantation 2015; Jan; 99 (01) 139-44
    CrossrefPubMedSuche in Google Scholar
  • 26 Elde S, Brubaker AL, Than PA. et al. Operative technique of donor organ procurement for en bloc heart-liver transplantation. Transplantation 2021; 105 (12) 2661-2665
    CrossrefPubMedSuche in Google Scholar
  • 27 Vaikunth SS, Concepcion W, Daugherty T. et al. Short-term outcomes of en bloc combined heart and liver transplantation in the failing Fontan. Clin Transplant 2019; 33 (06) e13540
    CrossrefPubMedSuche in Google Scholar
  • 28 Daly RC, Pereira NL, Taner T. et al. Combined heart and liver transplantation in highly sensitized patients: protection of the cardiac allograft from antibody mediated rejection by initial liver implantation. J Heart Lung Transplant 2017; 36 :Suppl S200
    PubMedSuche in Google Scholar
  • 29 McGiffin DC, Kure CE, Macdonald PS. et al. Hypothermic oxygenated perfusion (HOPE) safely and effectively extends acceptable donor heart preservation times: results of the Australian and New Zealand trial. J Heart Lung Transplant 2024; 43 (03) 485-495
    CrossrefPubMedSuche in Google Scholar
  • 30 Schlegel A, Mueller M, Muller X. et al. A multicenter randomized-controlled trial of hypothermic oxygenated perfusion (HOPE) for human liver grafts before transplantation. J Hepatol 2023; 78 (04) 783-793
    CrossrefPubMedSuche in Google Scholar
  • 31 Kransdorf EP, Kittleson MM, Benck LR. et al. Predicted heart mass is the optimal metric for size match in heart transplantation. J Heart Lung Transplant 2019; 38 (02) 156-165
    CrossrefPubMedSuche in Google Scholar
  • 32 Welz F, Schoenrath F, Friedrich A. et al. Acute kidney injury after heart transplantation: risk factors and clinical outcomes. J Cardiothorac Vasc Anesth 2024; 38 (05) 1150-1160
    CrossrefPubMedSuche in Google Scholar
  • 33 Nompleggi DJ, Bonkovsky HL. Nutritional supplementation in chronic liver disease: an analytical review. Hepatology 1994; 19 (02) 518-533
    CrossrefPubMedSuche in Google Scholar
  • 34 Frountzas M, Karampetsou N, Nikolaou C. et al. Combined heart and liver transplantation: an updated systematic review. Ann R Coll Surg Engl 2022; 104 (02) 88-94
    CrossrefPubMedSuche in Google Scholar
  • 35 Zhao K, Mclean RC, Hoteit MA, Olthoff KM. Combined heart and liver transplant: indication, patient selection, and allocation policy. Clin Liver Dis (Hoboken) 2019; 13 (06) 170-175
    CrossrefPubMedSuche in Google Scholar
  • 36 Just IA, Guelfirat M, Leser L. et al. Diagnostic and prognostic value of a TDI-derived systolic wall motion analysis as a screening modality for allograft rejection after heart transplantation. Life (Basel) 2021; 11 (11) 11
    PubMedSuche in Google Scholar
  • 37 Toledano MB, Mukherjee SK, Howell J. et al. The emerging burden of liver disease in cystic fibrosis patients: a UK nationwide study. PLoS One 2019; 14 (04) e0212779
    CrossrefPubMedSuche in Google Scholar
  • 38 Colombo C, Battezzati PM, Crosignani A. et al. Liver disease in cystic fibrosis: a prospective study on incidence, risk factors, and outcome. Hepatology 2002; 36 (06) 1374-1382
    CrossrefPubMedSuche in Google Scholar
  • 39 Deutsche Gesellschaft f ür Gastroenterologie, Verdauungs- und Stoffwechselkrankheiten (DGVS), Deutsche Gesellschaft f ür Allgemein- und Viszeralchirurgie (DGAV). Lebertransplantation 2023. Available at: https://www.dgvs.de/wp-content/uploads/2024/07/LL-LTX-v1.0-Leitlinie_15.07.2024_final.pdf
    PubMed
  • 40 Weill D, Benden C, Corris PA. et al. A consensus document for the selection of lung transplant candidates: 2014–an update from the Pulmonary Transplantation Council of the International Society for Heart and Lung Transplantation. J Heart Lung Transplant 2015; 34 (01) 1-15
    CrossrefPubMedSuche in Google Scholar
  • 41 Aburahma K, Salman J, Engel B. et al. Liver-first strategy for a combined lung and liver transplant in patients with cystic fibrosis. Eur J Cardiothorac Surg 2021; 60 (04) 822-830
    CrossrefPubMedSuche in Google Scholar
  • 42 Ceulemans LJ, Vos R, Neyrinck A, Pirenne J, Warnecke G, Van Raemdonck D. Liver-first versus lung-first: a new dilemma in combined organ transplantation. Transpl Int 2018; 31 (02) 230-231
    CrossrefPubMedSuche in Google Scholar
  • 43 Grannas G, Neipp M, Hoeper MM. et al. Indications for and outcomes after combined lung and liver transplantation: a single-center experience on 13 consecutive cases. Transplantation 2008; 85 (04) 524-531
    CrossrefPubMedSuche in Google Scholar
  • 44 Salman J, Grannas G, Ius F. et al. The liver-first approach for combined lung and liver transplantation. Eur J Cardiothorac Surg 2018; 54 (06) 1122-1127
    CrossrefPubMedSuche in Google Scholar
  • 45 Couetil JP, Houssin DP, Soubrane O. et al. Combined lung and liver transplantation in patients with cystic fibrosis. A 4 1/2-year experience. J Thorac Cardiovasc Surg 1995; 110 (05) 1415-1422 , discussion 1422–1423
    CrossrefPubMedSuche in Google Scholar
  • 46 Yi SG, Burroughs SG, Loebe M. et al. Combined lung and liver transplantation: analysis of a single-center experience. Liver Transpl 2014; 20 (01) 46-53
    CrossrefPubMedSuche in Google Scholar
  • 47 Han JL, Beal EW, Mumtaz K, Washburn K, Black SM. Combined liver-lung transplantation: Indications, outcomes, current experience and ethical issues. Transplant Rev (Orlando) 2019; 33 (02) 99-106
    CrossrefPubMedSuche in Google Scholar
  • 48 Margreiter R, Kramar R, Huber C. et al. Combined liver and kidney transplantation. Lancet 1984; 1 (8385) 1077-1078
    CrossrefPubMedSuche in Google Scholar
  • 49 Ekser B, Contreras AG, Andraus W, Taner T. Current status of combined liver-kidney transplantation. Int J Surg 2020; 82S: 149-154
    CrossrefPubMedSuche in Google Scholar
  • 50 Molema F, Martinelli D, Hörster F. et al; additional individual contributors of MetabERN. Liver and/or kidney transplantation in amino and organic acid-related inborn errors of metabolism: an overview on European data. J Inherit Metab Dis 2021; 44 (03) 593-605
    CrossrefPubMedSuche in Google Scholar
  • 51 Cullaro G, Hirose R, Lai JC. Changes in simultaneous liver-kidney transplant allocation policy may impact postliver transplant outcomes. Transplantation 2019; 103 (05) 959-964
    CrossrefPubMedSuche in Google Scholar
  • 52 Arroyo V, Angeli P, Moreau R. et al; investigators from the EASL-CLIF Consortium, Grifols Chair and European Foundation for the Study of Chronic Liver Failure (EF-Clif). The systemic inflammation hypothesis: towards a new paradigm of acute decompensation and multiorgan failure in cirrhosis. J Hepatol 2021; 74 (03) 670-685
    CrossrefPubMedSuche in Google Scholar
  • 53 Appenrodt B, Lammert F. Renal failure in patients with liver cirrhosis: novel classifications, biomarkers, treatment. Visc Med 2018; 34 (04) 246-252
    CrossrefPubMedSuche in Google Scholar
  • 54 Tariq R, Hadi Y, Chahal K, Reddy S, Salameh H, Singal AK. Incidence, mortality and predictors of acute kidney injury in patients with cirrhosis: a systematic review and meta-analysis. J Clin Transl Hepatol 2020; 8 (02) 135-142
    CrossrefPubMedSuche in Google Scholar
  • 55 Goudsmit BFJ, Putter H, Tushuizen ME. et al. Refitting the model for end-stage liver disease for the eurotransplant region. Hepatology 2021; 74 (01) 351-363
    CrossrefPubMedSuche in Google Scholar
  • 56 Formica RN, Aeder M, Boyle G. et al. Simultaneous liver-kidney allocation policy: a proposal to optimize appropriate utilization of scarce resources. Am J Transplant 2016; 16 (03) 758-766
    CrossrefPubMedSuche in Google Scholar
  • 57 Yazawa M, Maliakkal B, Nair S. et al. Longitudinal renal function in liver transplant recipients with acute-on-chronic liver failure. Clin Transl Gastroenterol 2020; 11 (06) e00185
    CrossrefPubMedSuche in Google Scholar
  • 58 Piano S, Romano A, Di Pascoli M, Angeli P. Why and how to measure renal function in patients with liver disease. Liver Int 2017; 37 (Suppl. 01) 116-122
    CrossrefPubMedSuche in Google Scholar
  • 59 Nagai S, Safwan M, Collins K. et al. Liver alone or simultaneous liver-kidney transplant? Pretransplant chronic kidney disease and post-transplant outcome - a retrospective study. Transpl Int 2018; 31: 1028-1040
    CrossrefPubMedSuche in Google Scholar
  • 60 Sharma P, Sui Z, Zhang M. et al. Renal outcomes after simultaneous liver-kidney transplantation: results from the US Multicenter Simultaneous Liver-Kidney Transplantation Consortium. Liver Transpl 2021; 27 (08) 1144-1153
    CrossrefPubMedSuche in Google Scholar
  • 61 Molnar MZ, Joglekar K, Jiang Y. et al; Global NAFLD Consortium. Association of pretransplant renal function with liver graft and patient survival after liver transplantation in patients with nonalcoholic steatohepatitis. Liver Transpl 2019; 25 (03) 399-410
    CrossrefPubMedSuche in Google Scholar
  • 62 Das A, Taner T, Kim J, Emamaullee J. Crossmatch, donor-specific antibody testing, and immunosuppression in simultaneous liver and kidney transplantation: a review. Transplantation 2021; 105 (12) e285-e291
    CrossrefPubMedSuche in Google Scholar
  • 63 Weeks SR, Luo X, Toman L. et al. Steroid-sparing maintenance immunosuppression is safe and effective after simultaneous liver-kidney transplantation. Clin Transplant 2020; 34 (10) e14036
    CrossrefPubMedSuche in Google Scholar
  • 64 AbdulRahim N, Anderson L, Kotla S. et al. Lack of benefit and potential harm of induction therapy in simultaneous liver-kidney transplants. Liver Transpl 2019; 25 (03) 411-424
    CrossrefPubMedSuche in Google Scholar
  • 65 Cullaro G, Sharma P, Jo J. et al. Temporal trends and evolving outcomes after simultaneous liver-kidney transplantation: results from the US SLKT Consortium. Liver Transpl 2021; 27 (11) 1613-1622
    CrossrefPubMedSuche in Google Scholar
  • 66 Bouari S, Rijkse E, Metselaar HJ. et al. A comparison between combined liver kidney transplants to liver transplants alone: a systematic review and meta-analysis. Transplant Rev (Orlando) 2021; 35 (04) 100633
    CrossrefPubMedSuche in Google Scholar
  • 67 Tinti F, Mitterhofer AP, Umbro I. et al. Combined liver-kidney transplantation versus liver transplant alone based on KDIGO stratification of estimated glomerular filtration rate: data from the United Kingdom Transplant registry - a retrospective cohort study. Transpl Int 2019; 32 (09) 918-932
    CrossrefPubMedSuche in Google Scholar
  • 68 Singal AK, Ong S, Satapathy SK, Kamath PS, Wiesner RH. Simultaneous liver kidney transplantation. Transpl Int 2019; 32 (04) 343-352
    CrossrefPubMedSuche in Google Scholar
  • 69 Ruiz R, Kunitake H, Wilkinson AH. et al. Long-term analysis of combined liver and kidney transplantation at a single center. Arch Surg 2006; 141 (08) 735-741 , discussion 741–742
    CrossrefPubMedSuche in Google Scholar
  • 70 Reyes JD. Intestinal transplantation: an unexpected journey. Robert E. Gross Lecture. J Pediatr Surg 2014; 49 (01) 13-18
    CrossrefPubMedSuche in Google Scholar
  • 71 Woodward JM, Massey D, Sharkey L. The Long and Short of IT: intestinal failure-associated liver disease (IFALD) in adults-recommendations for early diagnosis and intestinal transplantation. Frontline Gastroenterol 2020; 11 (01) 34-39
    CrossrefPubMedSuche in Google Scholar
  • 72 Lal S, Pironi L, Wanten G. et al; Home Artificial Nutrition & Chronic Intestinal Failure Special Interest Group of the European Society for Clinical Nutrition and Metabolism (ESPEN). Clinical approach to the management of Intestinal Failure Associated Liver Disease (IFALD) in adults: a position paper from the Home Artificial Nutrition and Chronic Intestinal Failure Special Interest Group of ESPEN. Clin Nutr 2018; 37 (6, Pt A): 1794-1797
    CrossrefPubMedSuche in Google Scholar
  • 73 Hawksworth JS, Desai CS, Khan KM. et al. Visceral transplantation in patients with intestinal-failure associated liver disease: evolving indications, graft selection, and outcomes. Am J Transplant 2018; 18 (06) 1312-1320
    CrossrefPubMedSuche in Google Scholar
  • 74 Rutter CS, Amin I, Russell NK, Sharkey LM, Butler AJ, Middleton SJ. Adult intestinal and multivisceral transplantation: experience from a single center in the United Kingdom. Transplant Proc 2016; 48 (02) 468-472
    CrossrefPubMedSuche in Google Scholar
  • 75 Tzakis AG, Kato T, Levi DM. et al. 100 multivisceral transplants at a single center. Ann Surg 2005; 242 (04) 480-490 , discussion 491–493
    CrossrefPubMedSuche in Google Scholar
  • 76 Abu-Elmagd K, Reyes J, Bond G. et al. Clinical intestinal transplantation: a decade of experience at a single center. Ann Surg 2001; 234 (03) 404-416 , discussion 416–417
    CrossrefPubMedSuche in Google Scholar
  • 77 Lamprecht G, Pape UF, Witte M, Pascher A. S3-Leitlinie der Deutschen Gesellschaft für Ernährungsmedizin e. V. in Zusammenarbeit mit der AKE, der GESKES und der DGVS. Aktuel Ernahrungsmed 2014; 39: e57-e71
    Thieme ConnectPubMedSuche in Google Scholar
  • 78 Vianna RM, Mangus RS, Kubal C, Fridell JA, Beduschi T, Tector AJ. Multivisceral transplantation for diffuse portomesenteric thrombosis. Ann Surg 2012; 255 (06) 1144-1150
    CrossrefPubMedSuche in Google Scholar
  • 79 Pruett TL, Tibell A, Alabdulkareem A. et al. The ethics statement of the Vancouver Forum on the live lung, liver, pancreas, and intestine donor. Transplantation 2006; 81 (10) 1386-1387
    CrossrefPubMedSuche in Google Scholar
  • 80 Bababekov YJ, Pomfret EA. Ethical considerations for simultaneous vs sequential liver-kidney donation from the same live donor: donor(s) selection is key. Gastroenterology 2024; 166 (03) 365-368
    CrossrefPubMedSuche in Google Scholar
  • 81 Marujo WC, Barros MF, Cury RA, Pacheco-Silva A, Sette Jr H. Successful combined kidney-liver right lobe transplant from a living donor. Lancet 1999; 353 (9153) 641
    CrossrefPubMedSuche in Google Scholar
  • 82 Gautier S, Monakhov A, Miloserdov I. et al. Simultaneous laparoscopic left lateral sectionectomy and nephrectomy in the same living donor: the first case report. Am J Transplant 2019; 19 (06) 1847-1851
    CrossrefPubMedSuche in Google Scholar
  • 83 Yankol Y, Karataş C, Kanmaz T, Koçak B, Kalayoğlu M, Acarlı K. Extreme living donation: a single center simultaneous and sequential living liver-kidney donor experience with long-term outcomes under literature review. Turk J Surg 2021; 37 (03) 207-214
    CrossrefPubMedSuche in Google Scholar
  • 84 Gautier S, Monakhov A, Tsiroulnikova O. et al. Deceased vs living donor grafts for pediatric simultaneous liver-kidney transplantation: a single-center experience. J Clin Lab Anal 2020; 34 (06) e23219
    CrossrefPubMedSuche in Google Scholar
  • 85 Gruessner RWG, Gruessner AC. Dual living donor organ transplants. Clin Transplant 2023; 37 (04) e14923
    CrossrefPubMedSuche in Google Scholar
  • 86 Testa G, Holterman M, Abcarian H, Iqbal R, Benedetti E. Simultaneous or sequential combined living donor-intestine transplantation in children. Transplantation 2008; 85 (05) 713-717
    CrossrefPubMedSuche in Google Scholar
  • 87 Testa G, Holterman M, John E, Kecskes S, Abcarian H, Benedetti E. Combined living donor liver/small bowel transplantation. Transplantation 2005; 79 (10) 1401-1404
    CrossrefPubMedSuche in Google Scholar
  • 88 Czigany Z, Lurje I, Schmelzle M. et al. Ischemia-reperfusion injury in marginal liver grafts and the role of hypothermic machine perfusion: molecular mechanisms and clinical implications. J Clin Med 2020; 9 (03) 9
    CrossrefPubMedSuche in Google Scholar
  • 89 Pandya K, Sastry V, Panlilio MT. et al. Differential impact of extended criteria donors after brain death or circulatory death in adult liver transplantation. Liver Transpl 2020; 26 (12) 1603-1617
    CrossrefPubMedSuche in Google Scholar
  • 90 Czigany Z, Lurje I, Tolba RH, Neumann UP, Tacke F, Lurje G. Machine perfusion for liver transplantation in the era of marginal organs-New kids on the block. Liver Int 2019; 39 (02) 228-249
    CrossrefPubMedSuche in Google Scholar
  • 91 Eshmuminov D, Becker D, Bautista Borrego L. et al. An integrated perfusion machine preserves injured human livers for 1 week. Nat Biotechnol 2020; 38 (02) 189-198
    CrossrefPubMedSuche in Google Scholar
  • 92 Czigany Z, Pratschke J, Froněk J. et al. Hypothermic oxygenated machine perfusion reduces early allograft injury and improves post-transplant outcomes in extended criteria donation liver transplantation from donation after brain death: results from a multicenter randomized controlled trial (HOPE ECD-DBD). Ann Surg 2021; 274 (05) 705-712
    CrossrefPubMedSuche in Google Scholar
  • 93 Nasralla D, Coussios CC, Mergental H. et al; Consortium for Organ Preservation in Europe. A randomized trial of normothermic preservation in liver transplantation. Nature 2018; 557 (7703) 50-56
    CrossrefPubMedSuche in Google Scholar
  • 94 Czigany Z, Uluk D, Pavicevic S. et al. Improved outcomes after hypothermic oxygenated machine perfusion in liver transplantation-Long-term follow-up of a multicenter randomized controlled trial. Hepatol Commun 2024; 8 (02) e0376
    CrossrefPubMedSuche in Google Scholar
  • 95 Schlegel A, Muller X, Mueller M. et al. Hypothermic oxygenated perfusion protects from mitochondrial injury before liver transplantation. EBioMedicine 2020; 60: 103014
    CrossrefPubMedSuche in Google Scholar
  • 96 Stone JP, Critchley WR, Major T. et al. Altered immunogenicity of donor lungs via removal of passenger leukocytes using ex vivo lung perfusion. Am J Transplant 2016; 16 (01) 33-43
    CrossrefPubMedSuche in Google Scholar
  • 97 Schlegel A, Kron P, Graf R, Clavien PA, Dutkowski P. Hypothermic oxygenated perfusion (HOPE) downregulates the immune response in a rat model of liver transplantation. Ann Surg 2014; 260 (05) 931-937 , discussion 937–938
    CrossrefPubMedSuche in Google Scholar
  • 98 Kvietkauskas M, Leber B, Strupas K, Stiegler P, Schemmer P. Machine perfusion of extended criteria donor organs: immunological aspects. Front Immunol 2020; 11: 192
    CrossrefPubMedSuche in Google Scholar
  • 99 Jochmans I, Moers C, Smits JM. et al. Machine perfusion versus cold storage for the preservation of kidneys donated after cardiac death: a multicenter, randomized, controlled trial. Ann Surg 2010; 252 (05) 756-764
    CrossrefPubMedSuche in Google Scholar
  • 100 Hosgood SA, Callaghan CJ, Wilson CH. et al. Normothermic machine perfusion versus static cold storage in donation after circulatory death kidney transplantation: a randomized controlled trial. Nat Med 2023; 29 (06) 1511-1519
    CrossrefPubMedSuche in Google Scholar
  • 101 Meister FA, Czigany Z, Rietzler K. et al. Decrease of renal resistance during hypothermic oxygenated machine perfusion is associated with early allograft function in extended criteria donation kidney transplantation. Sci Rep 2020; 10 (01) 17726
    CrossrefPubMedSuche in Google Scholar
  • 102 Muller X, Schlegel A, Kron P. et al. Novel real-time prediction of liver graft function during hypothermic oxygenated machine perfusion before liver transplantation. Ann Surg 2019; 270 (05) 783-790
    CrossrefPubMedSuche in Google Scholar
  • 103 Raigani S, De Vries RJ, Carroll C. et al. Viability testing of discarded livers with normothermic machine perfusion: alleviating the organ shortage outweighs the cost. Clin Transplant 2020; 34 (11) e14069
    CrossrefPubMedSuche in Google Scholar
  • 104 Turco L, Garcia-Tsao G, Magnani I. et al. Cardiopulmonary hemodynamics and C-reactive protein as prognostic indicators in compensated and decompensated cirrhosis. J Hepatol 2018; 68 (05) 949-958
    CrossrefPubMedSuche in Google Scholar
  • 105 Ekser B, Mangus RS, Fridell W. et al. A novel approach in combined liver and kidney transplantation with long-term outcomes. Ann Surg 2017; 265 (05) 1000-1008
    CrossrefPubMedSuche in Google Scholar
  • 106 Chang A, Schaubel DE, Chen M, Abt PL, Bittermann T. Trends and outcomes of hypothermic machine perfusion preservation of kidney allografts in simultaneous liver and kidney transplantation in the United States. Transpl Int 2022; 35: 10345
    CrossrefPubMedSuche in Google Scholar
  • 107 Das I, Pham SM, Perry DK, Croome KP. The use of ex situ normothermic machine perfusion in combined cardiac and liver transplantation procedures. Transplant Direct 2024; 10 (02) e1574
    CrossrefPubMedSuche in Google Scholar
  • 108 Shamaa TM, Shamaa O, Crombez C. et al. The use of normothermic liver preservation in combined liver and lung transplantation: a single-center experience. Am J Transplant 2022; 22 (09) 2261-2264
    CrossrefPubMedSuche in Google Scholar
  • 109 Demetris AJ, Bellamy CO, Gandhi CR, Prost S, Nakanuma Y, Stolz DB. Functional immune anatomy of the liver-as an allograft. Am J Transplant 2016; 16 (06) 1653-1680
    CrossrefPubMedSuche in Google Scholar
  • 110 Abrol N, Jadlowiec CC, Taner T. Revisiting the liver's role in transplant alloimmunity. World J Gastroenterol 2019; 25 (25) 3123-3135
    CrossrefPubMedSuche in Google Scholar
  • 111 Lurje I, Hammerich L, Tacke F. Dendritic cell and T cell crosstalk in liver fibrogenesis and hepatocarcinogenesis: implications for prevention and therapy of liver cancer. Int J Mol Sci 2020; 21 (19) 21
    CrossrefPubMedSuche in Google Scholar
  • 112 Taner T, Park WD, Stegall MD. Unique molecular changes in kidney allografts after simultaneous liver-kidney compared with solitary kidney transplantation. Kidney Int 2017; 91 (05) 1193-1202
    CrossrefPubMedSuche in Google Scholar
  • 113 Taner T, Gustafson MP, Hansen MJ. et al. Donor-specific hypo-responsiveness occurs in simultaneous liver-kidney transplant recipients after the first year. Kidney Int 2018; 93 (06) 1465-1474
    CrossrefPubMedSuche in Google Scholar
  • 114 Olausson M, Mjörnstedt L, Nordén G. et al. Successful combined partial auxiliary liver and kidney transplantation in highly sensitized cross-match positive recipients. Am J Transplant 2007; 7 (01) 130-136
    CrossrefPubMedSuche in Google Scholar
  • 115 Topilsky Y, Raichlin E, Hasin T. et al. Combined heart and liver transplant attenuates cardiac allograft vasculopathy compared with isolated heart transplantation. Transplantation 2013; 95 (06) 859-865
    CrossrefPubMedSuche in Google Scholar
  • 116 Wong TW, Gandhi MJ, Daly RC. et al. Liver allograft provides immunoprotection for the cardiac allograft in combined heart-liver transplantation. Am J Transplant 2016; 16 (12) 3522-3531
    CrossrefPubMedSuche in Google Scholar
  • 117 Jimenez J, Kapadia SR, Yamani MH. et al. Cellular rejection and rate of progression of transplant vasculopathy: a 3-year serial intravascular ultrasound study. J Heart Lung Transplant 2001; 20 (04) 393-398
    CrossrefPubMedSuche in Google Scholar
  • 118 Wu G, Cruz Jr RJ. Liver-inclusive intestinal transplantation results in decreased alloimmune-mediated rejection but increased infection. Gastroenterol Rep (Oxf) 2018; 6 (01) 29-37
    CrossrefPubMedSuche in Google Scholar
  • 119 Cunningham EC, Sharland AF, Bishop GA. Liver transplant tolerance and its application to the clinic: can we exploit the high dose effect?. Clin Dev Immunol 2013; 2013: 419692
    CrossrefPubMedSuche in Google Scholar
  • 120 Gugenheim J, Amorosa L, Gigou M. et al. Specific absorption of lymphocytotoxic alloantibodies by the liver in inbred rats. Transplantation 1990; 50 (02) 309-313
    CrossrefPubMedSuche in Google Scholar
  • 121 Gugenheim J, Le Thai B, Rouger P. et al. Relationship between the liver and lymphocytotoxic alloantibodies in inbred rats. Specific absorption by nonparenchymal liver cells. Transplantation 1988; 45 (02) 474-478
    CrossrefPubMedSuche in Google Scholar
  • 122 Ramon DS, Troop DM, Kinard TN. et al. Alloantibodies after simultaneous liver-kidney transplant: a story of primary nonfunction, retransplantation, and antibody-mediated rejection. Am J Transplant 2022; 22 (03) 977-985
    CrossrefPubMedSuche in Google Scholar
  • 123 Rasmussen A, Davies HF, Jamieson NV, Evans DB, Calne RY. Combined transplantation of liver and kidney from the same donor protects the kidney from rejection and improves kidney graft survival. Transplantation 1995; 59 (06) 919-921
    CrossrefPubMedSuche in Google Scholar
  • 124 Fung J, Makowka L, Tzakis A. et al. Combined liver-kidney transplantation: analysis of patients with preformed lymphocytotoxic antibodies. Transplant Proc 1988; 20 (1, Suppl 1): 88-91
    PubMedSuche in Google Scholar
  • 125 Taner T, Heimbach JK, Rosen CB, Nyberg SL, Park WD, Stegall MD. Decreased chronic cellular and antibody-mediated injury in the kidney following simultaneous liver-kidney transplantation. Kidney Int 2016; 89 (04) 909-917
    CrossrefPubMedSuche in Google Scholar
  • 126 Dar W, Agarwal A, Watkins C. et al. Donor-directed MHC class I antibody is preferentially cleared from sensitized recipients of combined liver/kidney transplants. Am J Transplant 2011; 11 (04) 841-847
    CrossrefPubMedSuche in Google Scholar
  • 127 Billingham RE, Brent L, Medawar PB. Actively acquired tolerance of foreign cells. Nature 1953; 172 (4379) 603-606
    CrossrefPubMedSuche in Google Scholar
  • 128 Wood K, Sachs DH. Chimerism and transplantation tolerance: cause and effect. Immunol Today 1996; 17 (12) 584-587 , discussion 588
    CrossrefPubMedSuche in Google Scholar
  • 129 Kashiwagi N, Porter KA, Penn I, Brettschneider L, Starzl TE. Studies of homograft sex and of gamma globulin phenotypes after orthotopic homotransplantation of the human liver. Surg Forum 1969; 20: 374-376
    PubMedSuche in Google Scholar
  • 130 Austyn JM, Hankins DF, Larsen CP, Morris PJ, Rao AS, Roake JA. Isolation and characterization of dendritic cells from mouse heart and kidney. J Immunol 1994; 152 (05) 2401-2410
    CrossrefPubMedSuche in Google Scholar
  • 131 Perico N, Remuzzi G. Acquired transplant tolerance. Int J Clin Lab Res 1997; 27 (03) 165-177
    CrossrefPubMedSuche in Google Scholar
  • 132 Wood KJ. Passenger leukocytes and microchimerism: what role in tolerance induction?. Transplantation 2003; 75 (09) 17S-20S
    CrossrefPubMedSuche in Google Scholar
  • 133 Rao AS, Thomson AW, Shapiro R, Starzl TE. Chimerism after whole organ transplantation: its relationship to graft rejection and tolerance induction. Curr Opin Nephrol Hypertens 1994; 3 (06) 589-595
    CrossrefPubMedSuche in Google Scholar
  • 134 Starzl TE, Demetris AJ, Murase N, Thomson AW, Trucco M, Ricordi C. Donor cell chimerism permitted by immunosuppressive drugs: a new view of organ transplantation. Immunol Today 1993; 14 (06) 326-332
    CrossrefPubMedSuche in Google Scholar
  • 135 Sun J, McCaughan GW, Gallagher ND, Sheil AG, Bishop GA. Deletion of spontaneous rat liver allograft acceptance by donor irradiation. Transplantation 1995; 60 (03) 233-236
    CrossrefPubMedSuche in Google Scholar
  • 136 Sivasai KS, Alevy YG, Duffy BF. et al. Peripheral blood microchimerism in human liver and renal transplant recipients: rejection despite donor-specific chimerism. Transplantation 1997; 64 (03) 427-432
    CrossrefPubMedSuche in Google Scholar
  • 137 Bishop GA, Ierino FL, Sharland AF. et al. Approaching the promise of operational tolerance in clinical transplantation. Transplantation 2011; 91 (10) 1065-1074
    CrossrefPubMedSuche in Google Scholar
  • 138 Bowen DG, Zen M, Holz L, Davis T, McCaughan GW, Bertolino P. The site of primary T cell activation is a determinant of the balance between intrahepatic tolerance and immunity. J Clin Invest 2004; 114 (05) 701-712
    CrossrefPubMedSuche in Google Scholar
  • 139 Sarwal MM, Cecka JM, Millan MT, Salvatierra Jr O. United Network for Organ Sharing. Adult-size kidneys without acute tubular necrosis provide exceedingly superior long-term graft outcomes for infants and small children: a single center and UNOS analysis. Transplantation 2000; 70 (12) 1728-1736
    CrossrefPubMedSuche in Google Scholar
  • 140 Raichlin E, Kushwaha SS, Daly RC. et al. Combined heart and kidney transplantation provides an excellent survival and decreases risk of cardiac cellular rejection and coronary allograft vasculopathy. Transplant Proc 2011; 43 (05) 1871-1876
    CrossrefPubMedSuche in Google Scholar
  • 141 Rana A, Robles S, Russo MJ. et al. The combined organ effect: protection against rejection?. Ann Surg 2008; 248 (05) 871-879
    CrossrefPubMedSuche in Google Scholar
  • 142 Cunningham EC, Tay SS, Wang C. et al. Gene therapy for tolerance: high-level expression of donor major histocompatibility complex in the liver overcomes naive and memory alloresponses to skin grafts. Transplantation 2013; 95 (01) 70-77
    CrossrefPubMedSuche in Google Scholar
  • 143 Davies HS, Pollard SG, Calne RY. Soluble HLA antigens in the circulation of liver graft recipients. Transplantation 1989; 47 (03) 524-527
    CrossrefPubMedSuche in Google Scholar
  • 144 O'Leary JG, Demetris AJ, Friedman LS. et al. The role of donor-specific HLA alloantibodies in liver transplantation. Am J Transplant 2014; 14 (04) 779-787
    CrossrefPubMedSuche in Google Scholar
  • 145 Creput C, Le Friec G, Bahri R. et al. Detection of HLA-G in serum and graft biopsy associated with fewer acute rejections following combined liver-kidney transplantation: possible implications for monitoring patients. Hum Immunol 2003; 64 (11) 1033-1038
    CrossrefPubMedSuche in Google Scholar
  • 146 Ingelsten M, Gustafsson K, Olausson M, Haraldsson B, Karlsson-Parra A, Nyström J. Rapid increase of interleukin-10 plasma levels after combined auxiliary liver-kidney transplantation in presensitized patients. Transplantation 2014; 98 (02) 208-215
    CrossrefPubMedSuche in Google Scholar
  • 147 Ingelsten M, Gustafsson K, Oltean M. et al. Is indoleamine 2,3-dioxygenase important for graft acceptance in highly sensitized patients after combined auxiliary liver-kidney transplantation?. Transplantation 2009; 88 (07) 911-919
    CrossrefPubMedSuche in Google Scholar
  • 148 Dumontet E, Danger R, Vagefi PA. et al. Peripheral phenotype and gene expression profiles of combined liver-kidney transplant patients. Liver Int 2016; 36 (03) 401-409
    CrossrefPubMedSuche in Google Scholar
  • 149 Zabransky DJ, Nirschl CJ, Durham NM. et al. Phenotypic and functional properties of Helios+ regulatory T cells. PLoS One 2012; 7 (03) e34547
    CrossrefPubMedSuche in Google Scholar
  • 150 Himmel ME, MacDonald KG, Garcia RV, Steiner TS, Levings MK. Helios+ and Helios- cells coexist within the natural FOXP3+ T regulatory cell subset in humans. J Immunol 2013; 190 (05) 2001-2008
    CrossrefPubMedSuche in Google Scholar
  • 151 Kim YC, Bhairavabhotla R, Yoon J. et al. Oligodeoxynucleotides stabilize Helios-expressing Foxp3+ human T regulatory cells during in vitro expansion. Blood 2012; 119 (12) 2810-2818
    CrossrefPubMedSuche in Google Scholar
  • 152 Asch WS, Bia MJ. New organ allocation system for combined liver-kidney transplants and the availability of kidneys for transplant to patients with stage 4-5 CKD. Clin J Am Soc Nephrol 2017; 12 (05) 848-852
    CrossrefPubMedSuche in Google Scholar