Clinical evidence of outcomes following liver transplantation in patients with nonalcoholic steatohepatitis: an updated meta-analysis and systematic review
Open accessAbstract
OBJECTIVE: Nonalcoholic steatohepatitis (NASH) is a dramatically growing indication for liver transplantation (LT) worldwide and the posttransplant outcomes of NASH patients are currently under intensive investigation. This quantitative meta-analysis aimed to update the clinical evidence on outcomes of transplanted patients with NASH. METHODS: We performed a systematic review and meta-analysis of studies (published up to September 15, 2021) that focused on LT outcomes for NASH versus non-NASH patients. Random-effect meta-analysis was conducted to calculate pooled odds ratios (ORs) and 95% confidence intervals (CIs). Subgroup analyses based on crucial baseline clinical characteristics and leave-one-out sensitivity analyses were conducted to assess the robustness of the pooled results. Meta-regression was used to evaluate study-level demographic, clinical, and biochemical characteristics to identify potential confounders affecting patient survival. RESULTS: Twenty-two non-randomized comparative studies with 1,538 NASH and 6,014 non-NASH patients were included. 1- (OR, 0.94; 95% CI, 0.77-1.14), 3- (OR, 0.82; 95% CI, 1.00-1.22), and 5- (OR, 1.05; 95% CI, 0.84-1.31) year patient survival was equivalent between NASH and non-NASH recipients. NASH patients were associated with similar cardiovascular mortality (OR, 1.36; 95% CI, 0.89-2.09) and retransplantation rates (OR, 0.69; 95% CI, 1.03-1.53), lower graft failure-related mortality (OR, 0.11; 95% CI, 0.29-0.74), but higher sepsis-related mortality (OR, 1.53; 95% CI, 1.13-2.06). Meta-regression revealed that a higher proportion of patients with hepatocellular carcinoma (HCC) were associated with significantly superior overall patient survival at 1 (P = 0.044), 3 (P = 0.035) and 5 (P = 0.049) years after LT in NASH compared with non-NASH. CONCLUSIONS: This study shows no difference in posttransplant survival between NASH and non-NASH patients. Carefully selected patients with NASH-related HCC may benefit from LT. NASH recipients should be managed with caution posttransplant, especially regarding the potentially high risk of sepsis-related death.
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Long-term graft and recipient survival after liver transplantation do not differ in many retrospective and registry analyses between adults with MASLD and others.
“Despite the overall higher rate of risk factors in adults with MASLD, long-term graft and recipient survival after liver transplantation do not differ in many retrospective and registry analyses, 482,486,487 supporting that candidates with MASLD can be safely transplanted, if properly”
From EASL-EASD-EASO Clinical Practice Guidelines on the management of metabolic dysfunction-associated steatotic liver disease (MASLD). (2024) · cites this paper as [487]
Sections 3.2.2–3.2.3 report similar 3- and 5-year patient survival after transplantation for NASH and non-NASH recipients. The paper does not establish equivalent long-term graft survival: Section 3.3.3 instead reports lower graft failure-related mortality in the NASH group. Its comparison concerns NASH, which is narrower than MASLD. (LLM, conf=0.86)
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Cites
Measuring inconsistency in meta-analyses
Higgins, J. P. T., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003) · BMJ · doi:10.1136/bmj.327.7414.557 · Cited by 63,139 · see citing works
Bias in meta-analysis detected by a simple, graphical test
Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997) · BMJ · doi:10.1136/bmj.315.7109.629 · Cited by 56,722 · see citing works
Meta-analysis in clinical trials
DerSimonian, R., & Laird, N. (1986) · Controlled Clinical Trials · doi:10.1016/0197-2456(86)90046-2 · Cited by 39,552 · see citing works
The PRISMA 2020 Statement: An Updated Guideline for Reporting Systematic Reviews
Page, M. J., McKenzie, J. E., Bossuyt, P. M., Boutron, I., Hoffmann, T. C., Mulrow, C. D., Shamseer, L., Tetzlaff, J. M., Akl, E. A., Brennan, S. E., et al. (2021) · International Journal of Surgery · doi:10.1016/j.ijsu.2021.105906 · Cited by 11,748 · see citing works
Wan, X., Wang, W., Liu, J., & Tong, T. (2014) · BMC Medical Research Methodology · doi:10.1186/1471-2288-14-135 · Cited by 11,735 · see citing works
Younossi, Z. M., Koenig, A. B., Abdelatif, D., Fazel, Y., Henry, L., & Wymer, M. (2016) · Hepatology · doi:10.1002/hep.28431 · Cited by 10,781 · see citing works
Charlton, M., Burns, J. M., Pedersen, R. A., Watt, K. D. S., Heimbach, J. K., & Dierkhising, R. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.06.061 · Cited by 1,103 · see citing works
Younossi, Z. M., Stepanova, M., Ong, J. P., Trimble, G., Alqahtani, S. A., Younossi, I. M., Ahmed, A., Racila, A., & Henry, L. L. (2020) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2020.05.064 · Cited by 587 · see citing works
Haldar, D., Kern, B., Hodson, J., Armstrong, M. J., Adam, R., Berlakovich, G., Fritz, J., Feurstein, B., Popp, W., Karam, V., et al. (2019) · Journal of Hepatology · doi:10.1016/j.jhep.2019.04.011 · Cited by 313 · see citing works
Liver Transplantation for Nonalcoholic Steatohepatitis
Agopian, V. G., Kaldas, F. M., Hong, J. C., Whittaker, M., Holt, C., Rana, A. A., Zarrinpar, A., Petrowsky, H., Farmer, D. G., Yersiz, H., et al. (2012) · Annals of Surgery · doi:10.1097/sla.0b013e31826b4b7e · Cited by 227 · see citing works
Reddy, S. K., Steel, J. L., Chen, H., DeMateo, D. J., Cardinal, J. S., Behari, J., Humar, A., Marsh, W. J., Geller, D. A., & Tsung, A. (2011) · Hepatology · doi:10.1002/hep.25536 · Cited by 224 · see citing works
VanWagner, L. B., Bhave, M., Te, H. S., Feinglass, J., Alvarez, L., & Rinella, M. E. (2012) · Hepatology · doi:10.1002/hep.25855 · Cited by 220 · see citing works
Outcome After Liver Transplantation for NASH Cirrhosis
Malik, S. M., DeVera, M., Fontes, P., Shaikh, O. S., & Ahmad, J. (2009) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2009.02590.x · Cited by 206 · see citing works
Wang, X., Li, J., Riaz, D., Shi, G., Liu, C., & Dai, Y. (2013) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2013.09.023 · Cited by 200 · see citing works
Bhagat, V., Mindikoglu, A. L., Nudo, C. G., Schiff, E. R., Tzakis, A. G., & Regev, A. (2009) · Liver Transplantation · doi:10.1002/lt.21927 · Cited by 181 · see citing works
Afzali, A., Berry, K., & Ioannou, G. N. (2011) · Liver Transplantation · doi:10.1002/lt.22435 · Cited by 135 · see citing works
Houlihan, D. D., Armstrong, M. J., Davidov, Y., Hodson, J. A., Nightingale, P., Rowe, I. A. C., Paris, S., Gunson, B. K., Bramhall, S. R., Mutimer, D., et al. (2011) · Liver Transplantation · doi:10.1002/lt.22382 · Cited by 73 · see citing works
Holmer, M., Melum, E., Isoniemi, H., Ericzon, B., Castedal, M., Nordin, A. J., Schultz, N. A., Rasmussen, A., Line, P., Stal, P. I., et al. (2018) · Liver International · doi:10.1111/liv.13751 · Cited by 66 · see citing works
Kennedy, C., Redden, D. T., Gray, S. H., Eckhoff, D. E., Massoud, O. I., McGuire, B. M., Alkurdi, B., Bloomer, J. R., & DuBay, D. A. (2012) · HPB · doi:10.1111/j.1477-2574.2012.00497.x · Cited by 61 · see citing works
Nagai, S., Collins, K., Chau, L. C., Safwan, M., Rizzari, M. D., Yoshida, A., Abouljoud, M. S., & Moonka, D. (2019) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2019.04.033 · Cited by 60 · see citing works
Park, C. W., Tsai, N., & Wong, L. L. (2011) · Clinical Transplantation · doi:10.1111/j.1399-0012.2011.01497.x · Cited by 57 · see citing works
Barritt, A. S., Dellon, E. S., Kozłowski, T., Gerber, D. A., & Hayashi, P. H. (2010) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e3181eeaff0 · Cited by 57 · see citing works
Sadler, E. M., Mehta, N., Bhat, M., Ghanekar, A., Greig, P., Grant, D., Yao, F. Y. K., & Sapisochin, G. (2018) · Transplantation · doi:10.1097/tp.0000000000002043 · Cited by 54 · see citing works
Yong, J. N., Lim, W. H., Ng, C. H., Tan, D. J. H., Xiao, J., Tay, P. W. L., Lin, S. Y., Syn, N. L. X., Chew, N., Nah, B. K. Y., et al. (2021) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2021.11.014 · Cited by 54 · see citing works
Bertot, L. C., Jeffrey, G. P., Jacques, B., McCaughan, G. W., Crawford, M. W., Angus, P., Jones, R. M., Gane, E. J., MUNN, S. R., Macdonald, G. A., et al. (2019) · Liver Transplantation · doi:10.1002/lt.25361 · Cited by 52 · see citing works
Wong, R. J., Chou, C., Bonham, C. A., Concepcion, W., Esquivel, C. O., & Ahmed, A. (2014) · Clinical Transplantation · doi:10.1111/ctr.12364 · Cited by 46 · see citing works
Sourianarayanane, A., Arikapudi, S., McCullough, A. J., & Humar, A. (2017) · European Journal of Gastroenterology & Hepatology · doi:10.1097/meg.0000000000000820 · Cited by 39 · see citing works
Molnar, M. Z., Joglekar, K., Jiang, Y., Cholankeril, G. T., Abdul, M. K. M., Kedia, S., González, H. C., Ahmed, A., Singal, A. K., Bhamidimarri, K. R., et al. (2018) · Liver Transplantation · doi:10.1002/lt.25367 · Cited by 36 · see citing works
Self-citationKwong, A. J., Devuni, D., Wang, C., Boike, J. R., Jo, J., VanWagner, L. B., Serper, M., Jones, L., Sharma, R., Verna, E. C., et al. (2020) · Liver Transplantation · doi:10.1002/lt.25863 · Cited by 28 · see citing works
Castelló, B., Aguilera, V., Blázquez, M. T., Rubín, Á., García, M., Vinaixa, C., Benlloch, S., Sanjuán, F., Montalvá, E. M., López, R., et al. (2019) · Annals of Hepatology · doi:10.1016/j.aohep.2019.06.014 · Cited by 26 · see citing works
Kern, B., Feurstein, B., Fritz, J., Fabritius, C., Sucher, R., Graziadei, I. W., Bale, R. J., Tilg, H., Zoller, H., Newsome, P. N., et al. (2018) · European Journal of Gastroenterology & Hepatology · doi:10.1097/meg.0000000000001270 · Cited by 20 · see citing works
Tokodai, K., Karadagi, A., Kjaernet, F., Romano, A., Ericzon, B., & Nowak, G. (2019) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365521.2019.1577484 · Cited by 20 · see citing works
Unger, L. W., Herac, M., Staufer, K., Salat, A., Silberhumer, G. R., Hofmann, M., Trauner, M. A., Rasoul‐Rockenschaub, S., Soliman, T., Reiberger, T., et al. (2016) · European Journal of Gastroenterology & Hepatology · doi:10.1097/meg.0000000000000794 · Cited by 15 · see citing works
Danford, C. J., Iriana, S., Shen, C., Curry, M. P., & Lai, M. (2019) · Liver International · doi:10.1111/liv.14080 · Cited by 14 · see citing works
Herck, J. V., Verbeek, J., van Malenstein, H., Laleman, W., Cassiman, D. M., Verslype, C., der Merwe, V., Jochmans, I., Sainz‐Barriga, M., Monbaliu, D. R. L., et al. (2021) · Transplantation Proceedings · doi:10.1016/j.transproceed.2021.02.025 · Cited by 14 · see citing works
Holzner, M. L., Florman, S. S., Schwartz, M., & Tabrizian, P. (2021) · HPB · doi:10.1016/j.hpb.2021.08.943 · Cited by 14 · see citing works
Satapathy, S. K., Jiang, Y., Eason, J. D., Kedia, S., Wong, E., Singal, A. K., Tolley, E. A., Hathaway, D., Nair, S. P., & Vanatta, J. M. (2017) · Transplant International · doi:10.1111/tri.13001 · Cited by 11 · see citing works
Self-citationLiver Transplantation: the Role of Metabolic Syndrome
Davis, B. C., & Siddiqui, M. (2017) · Current treatment options in gastroenterology · doi:10.1007/s11938-017-0135-1 · Cited by 10 · see citing works
Predicting Long-term Survival After Liver Transplantation in Patients With NASH Cirrhosis
karnam, R. S., Mitsakakis, N., Saracino, G., Lilly, L., Asrani, S. K., & Bhat, M. (2021) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2021.01.021 · Cited by 9 · see citing works
O’Neill, S., Napetti, S., Cornateanu, S., Sutherland, A., Wigmore, S. J., Oniscu, G. C., & Adair, A. (2017) · HPB · doi:10.1016/j.hpb.2017.08.003 · Cited by 8 · see citing works
Flagged first, then by citations
1 of the 41 references couldn’t be matched to a known paper.
Research works printed but not linked: 2
- F. Ferla, I. Vella, A. Ficarelli, R. De Carlis, A. Lauterio, et al., Does NASH jeopardize liver transplant survival IN HCC patients? The niguarda experience, Transpl. Int. 34 (2021), 336-336.
- N.A. Piazza, A.K. Singal, Frequency of cardiovascular events and effect on survival in liver transplant recipients for cirrhosis due to alcoholic or nonalcoholic steatohepatitis, Exp Clin Transplant 14 (2016) 79-85, https://doi.org/10.6002/ ect.2015.0089. · DOI
Cited by
Sorted by citations
Tacke, F., Horn, P., Wai-Sun Wong, V., Ratziu, V., Bugianesi, E., Francque, S., Zelber-Sagi, S., Valenti, L., Roden, M., Schick, F., et al. (2024) · Journal of Hepatology · doi:10.1016/j.jhep.2024.04.031 · Cited by 2,210 · see citing works
(2024) · Obesity Facts · doi:10.1159/000539371 · Cited by 510 · see citing works
Macrophage metabolism in nonalcoholic fatty liver disease
Zhang, W., & Lang, R. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1257596 · Cited by 24 · see citing works
Czarnecka, K., Czarnecka, P., Tronina, O., Bączkowska, T., & Durlik, M. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13061719 · Cited by 6 · see citing works
Beyzaei, Z., Bagheri, Z., Karimzadeh, S., & Geramizadeh, B. (2025) · Transplantation Proceedings · doi:10.1016/j.transproceed.2025.05.031 · Cited by 1 · see citing works
Collagen matrix scaffolds: Future perspectives for the management of chronic liver diseases
Martínez‐Castillo, M., Altamirano-Mendoza, I., Zielinski, R. J., Priebe, W., Barba, M. C. P., & Gutiérrez‐Reyes, G. (2023) · World Journal of Clinical Cases · doi:10.12998/wjcc.v11.i6.1224 · Cited by 1 · see citing works
Villeret, F., & Dumortier, J. (2022) · Liver International · doi:10.1111/liv.15429 · Cited by 1 · see citing works
Predictors of mid‐term survival after liver transplantation in patients with NAFLD cirrhosis
Jiang, Y., Zhou, G., Zhu, Z., & Sun, L. (2022) · Liver International · doi:10.1111/liv.15427
Self-citationGangwani, M. K., Irfan, O., Aziz, M., Priyanka, F., Dahiya, D. S., Hayat, U., Jaber, F., Ali, H., Inamdar, S., & Sicilia, M. G. S. D. (2025) · ASIDE Gastroenterology · doi:10.71079/aside.gi.06262582
von Loeffelholz, C., & Elke, G. (2025) · Springer eBooks · doi:10.1007/978-3-032-00818-3_4
- Authors
- Zhou, G.-P., Jiang, Y.-Z., Sun, L.-Y., & Zhu, Z.-J.
- Affiliations
- Capital Medical University (CN)
- Corresponding author
- Sun, Li-Ying
- Zhu, Zhi-Jun
- Venue
- International Journal of Surgery
- Published
- 2022-08
- Volume
- 104
- Pages
- 106752
- ISSN
- 1743-9159 (ISSN-L)
- 1743-9191
- OpenAlex
- W4284699430
- Cited by
- 10
- References
- 41
- Citations by year
- 2025: 3 · 2024: 3 · 2023: 2 · 2022: 2
- FWCI
- 0.59
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- International Journal of Surgery (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Beijing Postdoctoral Science Foundation
- Topics
- Health Sciences › Medicine › Surgery › Organ Transplantation Techniques and Outcomes
- Health Sciences › Medicine › Epidemiology › Liver Disease Diagnosis and Treatment
- Health Sciences › Medicine › Hepatology › Liver Disease and Transplantation
- Keywords
- nonalcoholic steatohepatitis, liver transplantation, post-transplant outcomes, patient survival, graft failure, sepsis mortality, cardiovascular mortality, retransplantation, hepatocellular carcinoma, liver disease severity, post-transplant complications, liver fibrosis
- MeSH terms
- Carcinoma, Hepatocellular, Humans, Liver Neoplasms, Retrospective Studies, Liver Transplantation, Treatment Outcome, Sepsis, Non-alcoholic Fatty Liver Disease
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