The Outcomes of Liver Transplantation in Severe Metabolic Dysfunction-Associated Steatotic Liver Disease Patients
Abstract
:1. Introduction
2. Epidemiology
3. Outcomes
Study | N | Survival | MASH | Non-MASH | CC | HCV | HBV | AIH | ALD | PSC |
---|---|---|---|---|---|---|---|---|---|---|
Large database studies | ||||||||||
Charlton et al. [36] Period: 2001–2009 Data source: SRTR | 35,781 LT; 1959 MASH | 1 y | 84% | 87% | 86% | • | • | • | • | • |
3 y | 78% | 78% | 79% | • | • | • | • | • | ||
Karnam et al. [39]. Period: 2002–2019 Data source: SRTR | 6515 LT for MASH cirrhosis | 5 y | 79% | • | • | • | • | • | • | • |
Younossi et al. [40]. Period: 2002–2016 Data source: SRTR | 158,347 LT candidates due to HCC | 1 y (mortality) | 10.6% | • | • | 10.6% | 8.1% | 8.6% | • | • |
3 y (mortality) | 19.7% | • | • | 24.4% | 16.7% | 19.9% | • | • | ||
5 y (mortality) | 28.2% | • | • | 34.9% | 21.5% | 31.3% | • | • | ||
Afzali et al. [41] Period: 1997 to 2010 Data source: UNOS | 69,962 LT; 1810 were MASH recipients | 1 y | 87.6% | • | • | • | • | • | • | • |
3 y | 82.2% | • | • | • | • | • | • | • | ||
5 y | 76.7% | • | • | • | • | • | • | • | ||
Singal et al. [42] Period: 1994–2009 Data source: UNOS | 54,687 LT; 1358 were due to MASH cirrhosis | 1 y | 88.8% | 86.9% | 87.2% | 89.5% | • | • | 88.6% | 93.4% |
3 y | 85.4% | 82.4% | 79.9% | 84.5% | • | • | 83% | 89.7% | ||
5 y | 84.1% | 78.6% | 75.9% | 82.4% | • | • | 79.4% | 87.4% | ||
10 y | 84.1% | 78.6% | 75.9% | 82.4% | • | • | 79.4% | 87.4% | ||
Thuluuath et al. [43]. Period: 2002–2019 Data source: UNOS | Cryptogenic (3241 patients) and MASH (4089 patients) cirrhosis | 30 d | 97% | • | 96% | • | • | 96% | 97% | • |
1 y | 89% | • | 87% | • | • | 88% | 90% | • | ||
2 y | 86% | • | 85% | • | • | 86% | 88% | • | ||
3 y | 83% | • | 82% | • | • | 84% | 84% | • | ||
5 y | 77% | • | 77% | • | • | 79% | 78% | • | ||
10 y | 63% | • | 61% | • | • | 65% | 60% | • | ||
Cholankeril et al. [44]. Period: 2003–2014 Data source UNOS/OPTN | 63,061 LT, including 20782 HCV (32.96%) | 5 y | 77,81% | • | • | 72,15% | • | • | • | • |
Rajendran et al. [45]. Period: 2001–2009 Data source: UNOS | 35,781 LT, of which 1959 were MASH | 1 y | 84% | 87% | • | • | • | • | • | • |
3 y | 78% | 78% | • | • | • | • | • | • | ||
Kwong et al. [46]. Period: 2010–2016 Data source: REALT | 1023 LT, of which 207 (20.2%) were due to MASH cirrhosis | 1 y | 91.3% | 90.1% | • | • | • | • | • | • |
3 y | 83.3% | 81.5% | • | • | • | • | • | • | ||
Haldar et al. [47] Period: 2002–2016 Data source: ELTR | 68,950 LT and 2741 MASH recipients | 1 y | 84.1% | 86.2% | • | • | • | • | • | • |
2.5 y | 80.2% | 81.6% | • | • | • | • | • | • | ||
5 y | 73.4% | 75.4% | • | • | • | • | • | • | ||
10 y | 62.1% | 62.9% | • | • | • | • | • | • | ||
Jamil et al. [48]. Period: 2005–2019 Data source: SRTR | Over 80,000 LT | 10 y | 61% | • | • | • | • | • | • | • |
Nagai et al. [49]. Period: 2016–2018 Data source: OPTN/UNOS | 6344 LT for MASH, 17,037 for HCV, and 9279 for ALD | 1 y | 90.4% | • | • | 92.8% | • | • | • | • |
Single-center studies | ||||||||||
VanWagner et al. [50]. Period: 1993–2010 Data source: Northwestern Memorial Hospital and the University of Chicago Medical Center | 115 had MASH (or CC with known risk factors for MASH); 127 patients with alcohol-induced cirrhosis | 1 y | 81.3% | • | • | • | • | • | 88.1% | • |
3 y | 73.3% | • | • | • | • | • | 85.3% | • | ||
5 y | 60.3% | • | • | • | • | • | 68.8% | • | ||
Kennedy et al. [51]. Period: 1999–2009 Data source: University of Alabama at Birmingham | 129 recipients with MASH and 775 recipients were non-MASH | 1 y | 90% | 92% | • | • | • | • | • | • |
3 y | 88% | 86% | • | • | • | • | • | • | ||
5 y | 85% | 80% | • | • | • | • | • | • | ||
Malik et al. [52]. Period: 1997–2008 Data source: University of Pittsburgh School of Medicine | 2021 LT; 98 patients with MASH cirrhosis | 24 h mortality | 4.1% | 1–3% | • | • | • | • | • | • |
30 d mortality | 6.1% | 2–5% | • | • | • | • | • | • | ||
2 y mortality | 21.4% | 13–18% | • | • | • | • | • | • | ||
3 y mortality | 25.5% | 16–30% | • | • | • | • | • | • | ||
5 y mortality | 27.6% | 19–35% | • | • | • | • | • | • | ||
Bhagat et al. [53]. Period: 1997–2007 Data source: University of Miami | For CC with the MASH phenotype (71 patients) or alcoholic cirrhosis (83 patients) | 1 y | 82% | • | • | • | • | • | 92% | • |
3 y | 79% | • | • | • | • | • | 86% | • | ||
5 y | 75% | • | • | • | • | • | 86% | • | ||
9 y | 62% | • | • | • | • | • | 76% | • | ||
Sadler et al. [54]. Period: 2004–2014 Data source: University of Toronto and University of California San Francisco | 929 LT were due to HCC and 60 were due to HCC in MASH cirrhosis | 1 y | 98% | 95% | • | • | • | • | • | • |
3 y | 96% | 84% | • | • | • | • | • | • | ||
5 y | 80% | 78% | • | • | • | • | • | • | ||
Agopian et al. [55]. Period: 1993–2011 Data source: The University of California, Transplant and Liver Cancer Centers in Los Angeles | 144 adult MASH patients | 1 y | 84% | • | • | • | • | • | • | • |
3 y | 75% | • | • | • | • | • | • | • | ||
5 y | 70% | • | • | • | • | • | • | • | ||
Barrit et al. [56]. Period: 2004–2007 Data source: University of North Carolina Hospital | 118 LT, and 18% were due MASH cirrhosis | 30 d | 81% | 95% | • | • | • | • | • | • |
1 y | 76% | 83% | • | • | • | • | • | • | ||
3 y | 76% | 73% | • | • | • | • | • | • | ||
El Atrache et al. [57]. Period: 1996–2008 Data source: Henry Ford Hospital, Detroit | MASH (46 patients) and CC (37 patients) | 10 y | 80% | • | • | • | • | • | • | • |
Bhati et al. [58]. Period: 1995–2013 Data source: University of Maryland School of Medicine, Baltimore | 103 LT; 48 had MASH cirrhosis | 5 y | 86% | • | • | • | • | • | • | • |
10 y | 71% | • | • | • | • | • | • | • | ||
15 y | 51% | • | • | • | • | • | • | • | ||
Sanjeevi et al. [59]. Period: 2016–2018 Data source: University of Nebraska Medical | 71 MASH patients, and 6 of them had HCC | 1 y | 87.6% | • | • | • | • | • | • | • |
3 y | 82.2% | • | • | • | • | • | • | • | ||
5 y | 76.7% | • | • | • | • | • | • | • | ||
Holzner et al. [60]. Period: 2001–2017 Data source: School of Medicine at Mount Sinai, New York | 635 LT, of which 51 (8%) were MASH-HCC | 1 y | 92% | • | • | 86% | 93% | • | 88% | • |
3 y | 86% | • | • | 76% | 87% | • | 76% | • | ||
5 y | 80% | • | • | 65% | 83% | • | 69% | • | ||
Kakar et al. [61]. Period: 2000–2015 Data source: University of Pittsburgh | 226 patients with MASH | 1 y | 82% | • | • | • | • | • | • | • |
5 y | 73% | • | • | • | • | • | • | • | ||
7 y | 62% | • | • | • | • | • | • | • | ||
Yalamanchili et al. [62]. Period: 1986–2004 Data source: Baylor University Medical Center, Dallas | 2052 LT; 7% for MASH (the cohort of MASH patients were with CC) | 1 y | 85.6% | 86.3% | • | • | • | • | • | • |
5 y | 71.4% | 69.9% | • | • | • | • | • | • | ||
10 y | 56.5% | 52.7% | • | • | • | • | • | • | ||
20 y | 12.6% | 20.6% | • | • | • | • | • | • | ||
Kern et al. [63]. Period: 2002–2012 Data source: Medical University of Innsbruck, Austria | 513 LT; 12.7% for MASH cirrhosis | 1 y | 93.2% | • | • | • | • | • | • | • |
3 y | 78.5% | • | • | • | • | • | • | • | ||
5 y | 72.1% | • | • | • | • | • | • | • | ||
Castello et al. [64]. Period: 1997–2016 Data source: La Fe University Hospital, Valencia | 1986 LT; 40 (2%) were labelled as MASH-related | 1 y | 89% | • | • | • | • | • | 83% | • |
3 y | 89% | • | • | • | • | • | 78% | • | ||
5 y | 83% | • | • | • | • | • | 72% | • | ||
Heuer et al. [65]. Period: 2007–2011 Data source: University Hospital of Essen, Essen, Germany | 432 LT; 40 due MASH-induced cirrhosis | 4 y mortality | 60% | • | • | • | • | • | • | • |
Tokodai et al. [66]. Period: 2007–2017 Data source: Karolinska University Hospital, Stockholm, Sweden | 694 LT; 27 MASH patients; and 68 ALD patients | 1 y | 89% | • | • | • | • | • | 91% | • |
Tanaka et al. [67]. Period: 1996–2013 Data source: Japan | 425 living-donor LT; 7 due to MASH | 5.3 y | 100% | • | • | • | • | • | • | • |
Jothimani et al. [68]. Period: 2009–2019 Data source: Bharath Institute of Higher Education and Research; India | 1017 LT, of whom 396 had MASH cirrhosis | 1 y | 86.6% | • | • | 91.3% | 93.5% | • | 86% | • |
3 y | 81.8% | • | • | 86.1% | 88.5% | • | 82.9% | • | ||
5 y | 75.9% | • | • | 86.1% | 88.5% | • | 79.7% | • |
3.1. Large Database Studies
3.2. Single-Center Studies
4. Common Complications
4.1. Cause of Death
4.2. Recurrent MASLD
4.3. Metabolic Syndrome
4.4. Thrombosis and Cardiovascular Events
4.5. Malignancy
4.6. Infection
4.7. Therapy
5. Future Perspectives and Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
References
- Zelman, S. The Liver in Obesity. AMA Arch. Intern. Med. 1952, 90, 141–156. [Google Scholar] [CrossRef] [PubMed]
- Younossi, Z.M.; Stepanova, M.; Ong, J.; Trimble, G.; AlQahtani, S.; Younossi, I.; Ahmed, A.; Racila, A.; Henry, L. Nonalcoholic Steatohepatitis Is the Most Rapidly Increasing Indication for Liver Transplantation in the United States. Clin. Gastroenterol. Hepatol. 2021, 19, 580–589.e5. [Google Scholar] [CrossRef]
- Schaffner, F.; Thaler, H. Nonalcoholic Fatty Liver Disease. Prog. Liver Dis. 1986, 8, 283–298. [Google Scholar]
- Ludwig, J.; Viggiano, T.R.; McGill, D.B.; Oh, B.J. Nonalcoholic Steatohepatitis: Mayo Clinic Experiences with a Hitherto Unnamed Disease. Mayo Clin. Proc. 1980, 55, 434–438. [Google Scholar]
- Rinella, M.E.; Lazarus, J.V.; Ratziu, V.; Francque, S.M.; Sanyal, A.J.; Kanwal, F.; Romero, D.; Abdelmalek, M.F.; Anstee, Q.M.; Arab, J.P.; et al. A Multisociety Delphi Consensus Statement on New Fatty Liver Disease Nomenclature. Hepatology 2023, 29, 101133. [Google Scholar] [CrossRef]
- Neuschwander-Tetri, B.A. Non-Alcoholic Fatty Liver Disease. BMC Med. 2017, 15, 45. [Google Scholar] [CrossRef]
- Angulo, P. Nonalcoholic Fatty Liver Disease. N. Engl. J. Med. 2002, 346, 1221–1231. [Google Scholar] [CrossRef]
- Bugianesi, E.; Leone, N.; Vanni, E.; Marchesini, G.; Brunello, F.; Carucci, P.; Musso, A.; De Paolis, P.; Capussotti, L.; Salizzoni, M.; et al. Expanding the Natural History of Nonalcoholic Steatohepatitis: From Cryptogenic Cirrhosis to Hepatocellular Carcinoma. Gastroenterology 2002, 123, 134–140. [Google Scholar] [CrossRef] [PubMed]
- Tiniakos, D.G.; Vos, M.B.; Brunt, E.M. Nonalcoholic Fatty Liver Disease: Pathology and Pathogenesis. Annu. Rev. Pathol. Mech. Dis. 2010, 5, 145–171. [Google Scholar] [CrossRef]
- Malik, S.M.; Gupte, P.A.; de Vera, M.E.; Ahmad, J. Liver Transplantation in Patients with Nonalcoholic Steatohepatitis-Related Hepatocellular Carcinoma. Clin. Gastroenterol. Hepatol. 2009, 7, 800–806. [Google Scholar] [CrossRef]
- Anstee, Q.M.; Reeves, H.L.; Kotsiliti, E.; Govaere, O.; Heikenwalder, M. From NASH to HCC: Current Concepts and Future Challenges. Nat. Rev. Gastroenterol. Hepatol. 2019, 16, 411–428. [Google Scholar] [CrossRef]
- Eslam, M.; Newsome, P.N.; Sarin, S.K.; Anstee, Q.M.; Targher, G.; Romero-Gomez, M.; Zelber-Sagi, S.; Wai-Sun Wong, V.; Dufour, J.-F.; Schattenberg, J.M.; et al. A New Definition for Metabolic Dysfunction-Associated Fatty Liver Disease: An International Expert Consensus Statement. J. Hepatol. 2020, 73, 202–209. [Google Scholar] [CrossRef] [PubMed]
- Eslam, M.; Sanyal, A.J.; George, J.; Sanyal, A.; Neuschwander-Tetri, B.; Tiribelli, C.; Kleiner, D.E.; Brunt, E.; Bugianesi, E.; Yki-Järvinen, H.; et al. MAFLD: A Consensus-Driven Proposed Nomenclature for Metabolic Associated Fatty Liver Disease. Gastroenterology 2020, 158, 1999–2014.e1. [Google Scholar] [CrossRef]
- International Diabetes Federation (IDF). Available online: https://idf.org/ (accessed on 4 July 2023).
- Shulman, G.I. Cellular Mechanisms of Insulin Resistance. J. Clin. Investig. 2000, 106, 171–176. [Google Scholar] [CrossRef] [PubMed]
- Tarantino, G.; Finelli, C. What about Non-Alcoholic Fatty Liver Disease as a New Criterion to Define Metabolic Syndrome? World J. Gastroenterol. WJG 2013, 19, 3375–3384. [Google Scholar] [CrossRef]
- Musso, G.; Gambino, R.; Cassader, M.; Pagano, G. Meta-Analysis: Natural History of Non-Alcoholic Fatty Liver Disease (NAFLD) and Diagnostic Accuracy of Non-Invasive Tests for Liver Disease Severity. Ann. Med. 2011, 43, 617–649. [Google Scholar] [CrossRef] [PubMed]
- Bae, J.C.; Cho, Y.K.; Lee, W.Y.; Seo, H.I.; Rhee, E.J.; Park, S.E.; Park, C.Y.; Oh, K.W.; Sung, K.C.; Kim, B.I. Impact of Nonalcoholic Fatty Liver Disease on Insulin Resistance in Relation to HbA1c Levels in Nondiabetic Subjects. Off. J. Am. Coll. Gastroenterol. ACG 2010, 105, 2389. [Google Scholar] [CrossRef]
- Dongiovanni, P.; Stender, S.; Pietrelli, A.; Mancina, R.M.; Cespiati, A.; Petta, S.; Pelusi, S.; Pingitore, P.; Badiali, S.; Maggioni, M.; et al. Causal Relationship of Hepatic Fat with Liver Damage and Insulin Resistance in Nonalcoholic Fatty Liver. J. Intern. Med. 2018, 283, 356–370. [Google Scholar] [CrossRef]
- Manchanayake, J.; Chitturi, S.; Nolan, C.; Farrell, G.C. Postprandial Hyperinsulinemia Is Universal in Non-Diabetic Patients with Nonalcoholic Fatty Liver Disease. J. Gastroenterol. Hepatol. 2011, 26, 510–516. [Google Scholar] [CrossRef]
- Ford, E.S.; Giles, W.H.; Dietz, W.H. Prevalence of the Metabolic Syndrome Among US AdultsFindings From the Third National Health and Nutrition Examination Survey. JAMA 2002, 287, 356–359. [Google Scholar] [CrossRef]
- Flegal, K.M.; Carroll, M.D.; Ogden, C.L.; Curtin, L.R. Prevalence and Trends in Obesity Among US Adults, 1999–2008. JAMA 2010, 303, 235–241. [Google Scholar] [CrossRef] [PubMed]
- Mokdad, A.H.; Ford, E.S.; Bowman, B.A.; Dietz, W.H.; Vinicor, F.; Bales, V.S.; Marks, J.S. Prevalence of Obesity, Diabetes, and Obesity-Related Health Risk Factors, 2001. JAMA 2003, 289, 76–79. [Google Scholar] [CrossRef]
- Younossi, Z.M.; Golabi, P.; Paik, J.M.; Henry, A.; Van Dongen, C.; Henry, L. The Global Epidemiology of Nonalcoholic Fatty Liver Disease (NAFLD) and Nonalcoholic Steatohepatitis (NASH): A Systematic Review. Hepatology 2023, 77, 1335–1347. [Google Scholar] [CrossRef] [PubMed]
- Browning, J.D.; Szczepaniak, L.S.; Dobbins, R.; Nuremberg, P.; Horton, J.D.; Cohen, J.C.; Grundy, S.M.; Hobbs, H.H. Prevalence of Hepatic Steatosis in an Urban Population in the United States: Impact of Ethnicity. Hepatology 2004, 40, 1387–1395. [Google Scholar] [CrossRef]
- Bedogni, G.; Miglioli, L.; Masutti, F.; Tiribelli, C.; Marchesini, G.; Bellentani, S. Prevalence of and Risk Factors for Nonalcoholic Fatty Liver Disease: The Dionysos Nutrition and Liver Study. Hepatology 2005, 42, 44–52. [Google Scholar] [CrossRef] [PubMed]
- Fan, J.-G.; Zhu, J.; Li, X.-J.; Chen, L.; Li, L.; Dai, F.; Li, F.; Chen, S.-Y. Prevalence of and Risk Factors for Fatty Liver in a General Population of Shanghai, China. J. Hepatol. 2005, 43, 508–514. [Google Scholar] [CrossRef]
- Nomura, H.; Kashiwagi, S.; Hayashi, J.; Kajiyama, W.; Tani, S.; Goto, M. Prevalence of Fatty Liver in a General Population of Okinawa, Japan. Jpn. J. Med. 1988, 27, 142–149. [Google Scholar] [CrossRef] [PubMed]
- Adams, L.A.; Sanderson, S.; Lindor, K.D.; Angulo, P. The Histological Course of Nonalcoholic Fatty Liver Disease: A Longitudinal Study of 103 Patients with Sequential Liver Biopsies. J. Hepatol. 2005, 42, 132–138. [Google Scholar] [CrossRef]
- Garg, R.; Tripathy, D.; Dandona, P. Insulin Resistance as a Proinflammatory State: Mechanisms, Mediators, and Therapeutic Interventions. Curr. Drug Targets 2003, 4, 487–492. [Google Scholar] [CrossRef]
- Riazi, K.; Azhari, H.; Charette, J.H.; Underwood, F.E.; King, J.A.; Afshar, E.E.; Swain, M.G.; Congly, S.E.; Kaplan, G.G.; Shaheen, A.-A. The Prevalence and Incidence of NAFLD Worldwide: A Systematic Review and Meta-Analysis. Lancet Gastroenterol. Hepatol. 2022, 7, 851–861. [Google Scholar] [CrossRef]
- Estes, C.; Razavi, H.; Loomba, R.; Younossi, Z.; Sanyal, A.J. Modeling the Epidemic of Nonalcoholic Fatty Liver Disease Demonstrates an Exponential Increase in Burden of Disease. Hepatology 2018, 67, 123–133. [Google Scholar] [CrossRef]
- Burra, P.; Berenguer, M.; Pomfret, E. The ILTS Consensus Conference on NAFLD/NASH and Liver Transplantation: Setting the Stage. Transplantation 2019, 103, 19. [Google Scholar] [CrossRef]
- Wong, R.J.; Aguilar, M.; Cheung, R.; Perumpail, R.B.; Harrison, S.A.; Younossi, Z.M.; Ahmed, A. Nonalcoholic Steatohepatitis Is the Second Leading Etiology of Liver Disease Among Adults Awaiting Liver Transplantation in the United States. Gastroenterology 2015, 148, 547–555. [Google Scholar] [CrossRef]
- Noureddin, M.; Vipani, A.; Bresee, C.; Todo, T.; Kim, I.K.; Alkhouri, N.; Setiawan, V.W.; Tran, T.; Ayoub, W.S.; Lu, S.C.; et al. NASH Leading Cause of Liver Transplant in Women: Updated Analysis of Indications For Liver Transplant and Ethnic and Gender Variances. Am. J. Gastroenterol. 2018, 113, 1649–1659. [Google Scholar] [CrossRef] [PubMed]
- Charlton, M.R.; Burns, J.M.; Pedersen, R.A.; Watt, K.D.; Heimbach, J.K.; Dierkhising, R.A. Frequency and Outcomes of Liver Transplantation for Nonalcoholic Steatohepatitis in the United States. Gastroenterology 2011, 141, 1249–1253. [Google Scholar] [CrossRef] [PubMed]
- Stepanova, M.; Kabbara, K.; Mohess, D.; Verma, M.; Roche-Green, A.; AlQahtani, S.; Ong, J.; Burra, P.; Younossi, Z.M. Nonalcoholic Steatohepatitis Is the Most Common Indication for Liver Transplantation among the Elderly: Data from the United States Scientific Registry of Transplant Recipients. Hepatol. Commun. 2022, 6, 1506–1515. [Google Scholar] [CrossRef] [PubMed]
- Younossi, Z.M.; Koenig, A.B.; Abdelatif, D.; Fazel, Y.; Henry, L.; Wymer, M. Global Epidemiology of Nonalcoholic Fatty Liver Disease—Meta-Analytic Assessment of Prevalence, Incidence, and Outcomes. Hepatology 2016, 64, 73–84. [Google Scholar] [CrossRef]
- Karnam, R.S.; Mitsakakis, N.; Saracino, G.; Lilly, L.; Asrani, S.K.; Bhat, M. Predicting Long-Term Survival After Liver Transplantation in Patients With NASH Cirrhosis. Clin. Gastroenterol. Hepatol. 2022, 20, 704–705. [Google Scholar] [CrossRef]
- Younossi, Z.; Stepanova, M.; Ong, J.P.; Jacobson, I.M.; Bugianesi, E.; Duseja, A.; Eguchi, Y.; Wong, V.W.; Negro, F.; Yilmaz, Y.; et al. Nonalcoholic Steatohepatitis Is the Fastest Growing Cause of Hepatocellular Carcinoma in Liver Transplant Candidates. Clin. Gastroenterol. Hepatol. 2019, 17, 748–755.e3. [Google Scholar] [CrossRef]
- Afzali, A.; Berry, K.; Ioannou, G.N. Excellent Posttransplant Survival for Patients with Nonalcoholic Steatohepatitis in the United States. Liver Transpl. 2012, 18, 29–37. [Google Scholar] [CrossRef]
- Singal, A.K.; Guturu, P.; Hmoud, B.; Kuo, Y.-F.; Salameh, H.; Wiesner, R.H. Evolving Frequency and Outcomes of Liver Transplantation Based on Etiology of Liver Disease. Transplantation 2013, 95, 755–760. [Google Scholar] [CrossRef]
- Thuluvath, P.J.; Hanish, S.; Savva, Y. Liver Transplantation in Cryptogenic Cirrhosis: Outcome Comparisons Between NASH, Alcoholic, and AIH Cirrhosis. Transplantation 2018, 102, 656. [Google Scholar] [CrossRef]
- Cholankeril, G.; Wong, R.J.; Hu, M.; Perumpail, R.B.; Yoo, E.R.; Puri, P.; Younossi, Z.M.; Harrison, S.A.; Ahmed, A. Liver Transplantation for Nonalcoholic Steatohepatitis in the US: Temporal Trends and Outcomes. Dig. Dis. Sci. 2017, 62, 2915–2922. [Google Scholar] [CrossRef]
- Rajendran, L.; Murillo Perez, C.F.; Ivanics, T.; Claasen, M.P.A.W.; Hansen, B.E.; Wallace, D.; Yoon, P.D.; Sapisochin, G. Outcomes of Liver Transplantation in Non-Alcoholic Steatohepatitis (NASH) versus Non-NASH Associated Hepatocellular Carcinoma. HPB 2023, 25, 556–567. [Google Scholar] [CrossRef]
- Kwong, A.J.; Devuni, D.; Wang, C.; Boike, J.; Jo, J.; VanWagner, L.; Serper, M.; Jones, L.; Sharma, R.; Verna, E.C.; et al. Outcomes of Liver Transplantation Among Older Recipients With Nonalcoholic Steatohepatitis in a Large Multicenter US Cohort: The Re-Evaluating Age Limits in Transplantation Consortium. Liver Transpl. 2020, 26, 1492–1503. [Google Scholar] [CrossRef]
- Haldar, D.; Kern, B.; Hodson, J.; Armstrong, M.J.; Adam, R.; Berlakovich, G.; Fritz, J.; Feurstein, B.; Popp, W.; Karam, V.; et al. Outcomes of Liver Transplantation for Non-Alcoholic Steatohepatitis: A European Liver Transplant Registry Study. J. Hepatol. 2019, 71, 313–322. [Google Scholar] [CrossRef]
- Jamil, O.K.; Sandikçi, B.; Faust, N.; Cotter, T.G.; Paul, S.; di Sabato, D.; Fung, J.; Charlton, M. Relatively Poor Long-Term Outcomes Following Liver Transplantation for NASH in the United States. Transplantation 2022, 106, 2006–2018. [Google Scholar] [CrossRef]
- Nagai, S.; Collins, K.; Chau, L.C.; Safwan, M.; Rizzari, M.; Yoshida, A.; Abouljoud, M.S.; Moonka, D. Increased Risk of Death in First Year After Liver Transplantation Among Patients with Nonalcoholic Steatohepatitis vs Liver Disease of Other Etiologies. Clin. Gastroenterol. Hepatol. 2019, 17, 2759–2768.e5. [Google Scholar] [CrossRef]
- VanWagner, L.B.; Bhave, M.; Te, H.S.; Feinglass, J.; Alvarez, L.; Rinella, M.E. Patients Transplanted for Nonalcoholic Steatohepatitis Are at Increased Risk for Postoperative Cardiovascular Events. Hepatology 2012, 56, 1741–1750. [Google Scholar] [CrossRef]
- Kennedy, C.; Redden, D.; Gray, S.; Eckhoff, D.; Massoud, O.; McGuire, B.; Alkurdi, B.; Bloomer, J.; DuBay, D.A. Equivalent Survival Following Liver Transplantation in Patients with Non-Alcoholic Steatohepatitis Compared with Patients with Other Liver Diseases. HPB 2012, 14, 625–634. [Google Scholar] [CrossRef]
- Malik, S.M.; DeVera, M.E.; Fontes, P.; Shaikh, O.; Ahmad, J. Outcome After Liver Transplantation for NASH Cirrhosis. Am. J. Transplant. 2009, 9, 782–793. [Google Scholar] [CrossRef]
- Bhagat, V.; Mindikoglu, A.L.; Nudo, C.G.; Schiff, E.R.; Tzakis, A.; Regev, A. Outcomes of Liver Transplantation in Patients with Cirrhosis Due to Nonalcoholic Steatohepatitis versus Patients with Cirrhosis Due to Alcoholic Liver Disease: Outcome of Liver Transplantation for NASH. Liver Transpl. 2009, 15, 1814–1820. [Google Scholar] [CrossRef]
- Sadler, E.M.; Mehta, N.; Bhat, M.; Ghanekar, A.; Greig, P.D.; Grant, D.R.; Yao, F.; Sapisochin, G. Liver Transplantation for NASH-Related Hepatocellular Carcinoma Versus Non-NASH Etiologies of Hepatocellular Carcinoma. Transplantation 2018, 102, 640. [Google Scholar] [CrossRef] [PubMed]
- Agopian, V.G.; Kaldas, F.M.; Hong, J.C.; Whittaker, M.; Holt, C.; Rana, A.; Zarrinpar, A.; Petrowsky, H.; Farmer, D.; Yersiz, H.; et al. Liver Transplantation for Nonalcoholic Steatohepatitis: The New Epidemic. Ann. Surg. 2012, 256, 624. [Google Scholar] [CrossRef] [PubMed]
- Barritt, A.S.; Dellon, E.S.; Kozlowski, T.; Gerber, D.A.; Hayashi, P.H. The Influence of Nonalcoholic Fatty Liver Disease and Its Associated Comorbidities on Liver Transplant Outcomes. J. Clin. Gastroenterol. 2011, 45, 372–378. [Google Scholar] [CrossRef] [PubMed]
- El Atrache, M.M.; Abouljoud, M.S.; Divine, G.; Yoshida, A.; Kim, D.Y.; Kazimi, M.M.; Moonka, D.; Huang, M.A.; Brown, K. Recurrence of Non-Alcoholic Steatohepatitis and Cryptogenic Cirrhosis Following Orthotopic Liver Transplantation in the Context of the Metabolic Syndrome. Clin. Transplant. 2012, 26, E505–E512. [Google Scholar] [CrossRef]
- Bhati, C.; Idowu, M.O.; Sanyal, A.J.; Rivera, M.; Driscoll, C.; Stravitz, R.T.; Kohli, D.R.; Matherly, S.; Puri, P.; Gilles, H.; et al. Long-Term Outcomes in Patients Undergoing Liver Transplantation for Nonalcoholic Steatohepatitis-Related Cirrhosis. Transplantation 2017, 101, 1867. [Google Scholar] [CrossRef]
- Sanjeevi, A.; Lyden, E.; Sunderman, B.; Weseman, R.; Ashwathnarayan, R.; Mukherjee, S. Outcomes of Liver Transplantation for Cryptogenic Cirrhosis: A Single-Center Study of 71 Patients. Transplant. Proc. 2003, 35, 2977–2980. [Google Scholar] [CrossRef]
- Holzner, M.L.; Florman, S.; Schwartz, M.E.; Tabrizian, P. Outcomes of Liver Transplantation for Nonalcoholic Steatohepatitis-Associated Hepatocellular Carcinoma. HPB 2022, 24, 470–477. [Google Scholar] [CrossRef]
- Kakar, S.; Dugum, M.; Cabello, R.; Humar, A.; Ahmad, J.; Malik, S.M. Incidence of Recurrent NASH-Related Allograft Cirrhosis. Dig. Dis. Sci. 2019, 64, 1356–1363. [Google Scholar] [CrossRef]
- Yalamanchili, K.; Saadeh, S.; Klintmalm, G.B.; Jennings, L.W.; Davis, G.L. Nonalcoholic Fatty Liver Disease after Liver Transplantation for Cryptogenic Cirrhosis or Nonalcoholic Fatty Liver Disease: Fatty Liver Disease After Liver Transplantation. Liver Transpl. 2010, 16, 431–439. [Google Scholar] [CrossRef] [PubMed]
- Kern, B.; Feurstein, B.; Fritz, J.; Fabritius, C.; Sucher, R.; Graziadei, I.; Bale, R.; Tilg, H.; Zoller, H.; Newsome, P.; et al. High Incidence of Hepatocellular Carcinoma and Postoperative Complications in Patients with Nonalcoholic Steatohepatitis as a Primary Indication for Deceased Liver Transplantation. Eur. J. Gastroenterol. Hepatol. 2019, 31, 205–210. [Google Scholar] [CrossRef]
- Castelló, B.; Aguilera, V.; Blázquez, M.T.; Rubín, Á.; García, M.; Vinaixa, C.; Benlloch, S.; SanJuan, F.; Montalva, E.; López, R.; et al. Post-Transplantation Outcome in Non-Alcoholic Steatohepatitis Cirrhosis: Comparison with Alcoholic Cirrhosis. Ann. Hepatol. 2019, 18, 855–861. [Google Scholar] [CrossRef] [PubMed]
- Heuer, M.; Kaiser, G.M.; Kahraman, A.; Banysch, M.; Saner, F.H.; Mathé, Z.; Gerken, G.; Paul, A.; Canbay, A.; Treckmann, J.W. Liver Transplantation in Nonalcoholic Steatohepatitis Is Associated with High Mortality and Post-Transplant Complications: A Single-Center Experience. Gastroenterologia 2012, 86, 107–113. [Google Scholar] [CrossRef]
- Tokodai, K.; Karadagi, A.; Kjaernet, F.; Romano, A.; Ericzon, B.-G.; Nowak, G. Characteristics and Risk Factors for Recurrence of Nonalcoholic Steatohepatitis Following Liver Transplantation. Scand. J. Gastroenterol. 2019, 54, 233–239. [Google Scholar] [CrossRef]
- Tanaka, T.; Sugawara, Y.; Tamura, S.; Kaneko, J.; Takazawa, Y.; Aoki, T.; Hasegawa, K.; Sakamoto, Y.; Yamashiki, N.; Kokudo, N. Living Donor Liver Transplantation for Non-Alcoholic Steatohepatitis: A Single Center Experience. Hepatol. Res. 2014, 44, E3–E10. [Google Scholar] [CrossRef] [PubMed]
- Jothimani, D.; Danielraj, S.; Narasimhan, G.; Kaliamoorthy, I.; Rajakumar, A.; Palaniappan, K.; Palanichamy, S.; Rammohan, A.; Ramachandran, H.; Rajalingam, R.; et al. Nonalcoholic Steatohepatitis: A Rapidly Increasing Indication for Liver Transplantation in India. J. Clin. Exp. Hepatol. 2022, 12, 908–916. [Google Scholar] [CrossRef]
- Narayanan, P.; Mara, K.; Izzy, M.; Dierkhising, R.; Heimbach, J.; Allen, A.M.; Watt, K.D. Recurrent or De Novo Allograft Steatosis and Long-Term Outcomes After Liver Transplantation. Transplantation 2019, 103, e14. [Google Scholar] [CrossRef]
- Wang, X.; Li, J.; Riaz, D.R.; Shi, G.; Liu, C.; Dai, Y. Outcomes of Liver Transplantation for Nonalcoholic Steatohepatitis: A Systematic Review and Meta-Analysis. Clin. Gastroenterol. Hepatol. 2014, 12, 394–402.e1. [Google Scholar] [CrossRef]
- Watt, K.D. Metabolic Syndrome: Is Immunosuppression to Blame? Liver Transpl. 2011, 17, S38. [Google Scholar] [CrossRef] [PubMed]
- Contos, M.J.; Cales, W.; Sterling, R.K.; Luketic, V.A.; Shiffman, M.L.; Mills, A.S.; Fisher, R.A.; Ham, J.; Sanyal, A.J. Development of Nonalcoholic Fatty Liver Disease after Orthotopic Liver Transplantation for Cryptogenic Cirrhosis. Liver Transpl. 2001, 7, 363–373. [Google Scholar] [CrossRef] [PubMed]
- Dureja, P.; Mellinger, J.; Agni, R.; Chang, F.; Avey, G.; Lucey, M.; Said, A. NAFLD Recurrence in Liver Transplant Recipients. Transplantation 2011, 91, 684. [Google Scholar] [CrossRef] [PubMed]
- Ong, J.; Younossi, Z.M.; Reddy, V.; Price, L.L.; Gramlich, T.; Mayes, J.; Boparai, N. Cryptogenic Cirrhosis and Posttransplantation Nonalcoholic Fatty Liver Disease. Liver Transpl. 2001, 7, 797–801. [Google Scholar] [CrossRef] [PubMed]
- Charlton, M. Evolving Aspects of Liver Transplantation for Nonalcoholic Steatohepatitis. Curr. Opin. Organ. Transplant. 2013, 18, 251. [Google Scholar] [CrossRef]
- Andrade, A.R.; Bittencourt, P.L.; Codes, L.; Evangelista, M.A.; Castro, A.O.; Sorte, N.B.; Almeida, C.G.; Bastos, J.A.; Cotrim, H.P. New Onset Diabetes and Non-Alcoholic Fatty Liver Disease after Liver Transplantation. Ann. Hepatol. 2018, 16, 932–940. [Google Scholar] [CrossRef]
- Alkhouri, N.; Hanouneh, I.A.; Zein, N.N.; Lopez, R.; Kelly, D.; Eghtesad, B.; Fung, J.J. Liver Transplantation for Nonalcoholic Steatohepatitis in Young Patients. Transpl. Int. 2016, 29, 418–424. [Google Scholar] [CrossRef]
- Chauhan, K.; Khan, A.; Chowdhury, S.; Ross, H.M.; Parra, N.S.; Halegoua-DeMarzio, D. A Comprehensive Review on the Risk of Metabolic Syndrome and Cardiovascular Disease after Liver Transplantation. Livers 2022, 2, 85–96. [Google Scholar] [CrossRef]
- EBSCOhost|15071515|Role of Hypertension in Chronic Renal Allograft Dysfunction. Available online: https://web.p.ebscohost.com/abstract?direct=true&profile=ehost&scope=site&authtype=crawler&jrnl=00986577&AN=15071515&h=lrMW1nvtQ3UrEy54Rr3YfqQgYXIY9ee5YmTecGR8Kqh5Z8H4wmy9dumyS8%2bOziztHNGu4kSaSyZEHZus5vWQhg%3d%3d&crl=c&resultNs=AdminWebAuth&resultLocal=ErrCrlNotAuth&crlhashurl=login.aspx%3fdirect%3dtrue%26profile%3dehost%26scope%3dsite%26authtype%3dcrawler%26jrnl%3d00986577%26AN%3d15071515 (accessed on 22 August 2023).
- Seifeldin, R.; Marcos-Alvarez, A.; Lewis, W.D.; Gordon, F.D.; Jenkins, R.L. Effect of Nifedipine on Renal Function in Liver Transplant Recipients Receiving Tacrolimus. Clin. Ther. 1996, 18, 491–496. [Google Scholar] [CrossRef]
- Klintmalm, G.B.; Gonwa, T.A. Nephrotoxicity Associated with Cyclosporine and FK506. Liver Transplant. Surg. Off. Publ. Am. Assoc. Study Liver Dis. Int. Liver Transplant. Soc. 1995, 1, 11–19. [Google Scholar]
- Canzanello, V.J.; Textor, S.C.; Taler, S.J.; Schwartz, L.L.; Porayko, M.K.; Wiesner, R.H.; Krom, R.A.F. Late Hypertension after Liver Transplantation: A Comparison of Cyclosporine and Tacrolimus (FK 506). Liver Transpl. Surg. 1998, 4, 328–334. [Google Scholar] [CrossRef]
- Piazza, N.; Singal, A. Frequency of Cardiac Events and Impact on Survival Among Liver Transplant Recipients for Steatohepatitis-Related Cirrhosis: 471. Off. J. Am. Coll. Gastroenterol. ACG 2014, 109, S141. [Google Scholar] [CrossRef]
- Zarrinpar Metabolic Factors Affecting Hepatocellular Carcinoma in Steatohepatitis-Zarrinpar-2019-Liver International-Wiley Online Library. Available online: https://onlinelibrary.wiley.com/doi/abs/10.1111/liv.14002 (accessed on 4 August 2023).
- Gitto, S.; Villa, E. Non-Alcoholic Fatty Liver Disease and Metabolic Syndrome after Liver Transplant. Int. J. Mol. Sci. 2016, 17, 490. [Google Scholar] [CrossRef] [PubMed]
- Mikolasevic, I.; Orlic, L.; Hrstic, I.; Milic, S. Metabolic Syndrome and Non-Alcoholic Fatty Liver Disease after Liver or Kidney Transplantation. Hepatol. Res. 2016, 46, 841–852. [Google Scholar] [CrossRef] [PubMed]
- Sanyal, A.J.; Campbell–Sargent, C.; Mirshahi, F.; Rizzo, W.B.; Contos, M.J.; Sterling, R.K.; Luketic, V.A.; Shiffman, M.L.; Clore, J.N. Nonalcoholic Steatohepatitis: Association of Insulin Resistance and Mitochondrial Abnormalities. Gastroenterology 2001, 120, 1183–1192. [Google Scholar] [CrossRef] [PubMed]
- Newsome, P.N.; Allison, M.E.; Andrews, P.A.; Auzinger, G.; Day, C.P.; Ferguson, J.W.; Henriksen, P.A.; Hubscher, S.G.; Manley, H.; McKiernan, P.J.; et al. Guidelines for Liver Transplantation for Patients with Non-Alcoholic Steatohepatitis. Gut 2012, 61, 484–500. [Google Scholar] [CrossRef] [PubMed]
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Paklar, N.; Mijic, M.; Filipec-Kanizaj, T. The Outcomes of Liver Transplantation in Severe Metabolic Dysfunction-Associated Steatotic Liver Disease Patients. Biomedicines 2023, 11, 3096. https://doi.org/10.3390/biomedicines11113096
Paklar N, Mijic M, Filipec-Kanizaj T. The Outcomes of Liver Transplantation in Severe Metabolic Dysfunction-Associated Steatotic Liver Disease Patients. Biomedicines. 2023; 11(11):3096. https://doi.org/10.3390/biomedicines11113096
Chicago/Turabian StylePaklar, Natasa, Maja Mijic, and Tajana Filipec-Kanizaj. 2023. "The Outcomes of Liver Transplantation in Severe Metabolic Dysfunction-Associated Steatotic Liver Disease Patients" Biomedicines 11, no. 11: 3096. https://doi.org/10.3390/biomedicines11113096