Cited by 313Organ Transplantation Techniques and OutcomesLiver Disease Diagnosis and TreatmentLiver Disease and Transplantation

Outcomes of liver transplantation for non-alcoholic steatohepatitis: a European Liver Transplant Registry study

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Haldar, Debashis, Kern, Barbara, Hodson, James, Armstrong, Matthew James, Adam, Rene, Berlakovich, Gabriela, Fritz, Josef, Feurstein, Benedikt +19 more·2019·Journal of Hepatology

Abstract

Background & Aims Little is known about outcomes of liver transplantation for patients with non-alcoholic steatohepatitis (NASH). We aimed to determine the frequency and outcomes of liver transplantation for patients with NASH in Europe and identify prognostic factors. Methods We analysed data from patients transplanted for end-stage liver disease between January 2002 and December 2016 using the European Liver Transplant Registry database. We compared data between patients with NASH versus other aetiologies. The principle endpoints were patient and overall allograft survival. Results Among 68,950 adults undergoing first liver transplantation, 4.0% were transplanted for NASH – an increase from 1.2% in 2002 to 8.4% in 2016. A greater proportion of patients transplanted for NASH (39.1%) had hepatocellular carcinoma (HCC) than non-NASH patients (28.9%, p < 0.001). NASH was not significantly associated with survival of patients (hazard ratio [HR] 1.02, p = 0.713) or grafts (HR 0.99; p = 0.815) after accounting for available recipient and donor variables. Infection (24.0%) and cardio/cerebrovascular complications (5.3%) were the commonest causes of death in patients with NASH without HCC. Increasing recipient age (61–65 years: HR 2.07, p < 0.001; >65: HR 1.72, p = 0.017), elevated model for end-stage liver disease score (>23: HR 1.48, p = 0.048) and low (<18.5 kg/m 2 : HR 4.29, p = 0.048) or high (>40 kg/m 2 : HR 1.96, p = 0.012) recipient body mass index independently predicted death in patients transplanted for NASH without HCC. Data must be interpreted in the context of absent recognised confounders, such as pre-morbid metabolic risk factors. Conclusions The number and proportion of liver transplants performed for NASH in Europe has increased from 2002 through 2016. HCC was more common in patients transplanted with NASH. Survival of patients and grafts in patients with NASH is comparable to that of other disease indications. Lay summary The prevalence of non-alcoholic fatty liver disease has increased dramatically in parallel with the worldwide increase in obesity and diabetes. Its progressive form, non-alcoholic steatohepatitis, is a growing indication for liver transplantation in Europe, with good overall outcomes reported. However, careful risk factor assessment is required to maintain favourable post-transplant outcomes in patients with non-alcoholic steatohepatitis.

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Crossref · 10.1016/j.jhep.2019.04.011

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  • Infections (24%) and cardio/cerebrovascular complications (5.3%) were the commonest causes of death in individuals with MASH without HCC.

    “Infections (24%) and cardio/ cerebrovascular complications (5.3%) were the commonest causes of death in individuals with MASH without HCC. 482”

    From EASL-EASD-EASO Clinical Practice Guidelines on the management of metabolic dysfunction-associated steatotic liver disease (MASLD). (2024) · cites this paper as [482]

    The Results section, “Causes of death after liver transplantation,” reports infection (24.0%) and cardio/cerebrovascular complications (5.3%) as the top two known causes of death among NASH transplant recipients without HCC. The citing sentence omits that these figures apply to liver-transplant recipients and to known causes of death; 42.2% of deaths in the NASH group had unknown causes. (LLM, conf=0.88)

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  • Independent risk factors for death in individuals transplanted for MASH without HCC were recipient age, model for end-stage liver disease score and obesity.

    “Independent risk factors for death in individuals transplanted for MASH without HCC were recipient age, model for end-stage liver disease score and obesity. 482”

    From EASL-EASD-EASO Clinical Practice Guidelines on the management of metabolic dysfunction-associated steatotic liver disease (MASLD). (2024) · cites this paper as [482]

    The Results section and Table 3 identify older recipient age and MELD >23 as independent mortality risk factors after transplantation for NASH without HCC. They also find increased risk at BMI >40 kg/m², but not across all obesity categories; low BMI is associated with increased risk too. The claim's unqualified reference to obesity overstates the BMI finding. (LLM, conf=0.88)

    Experimental — accuracy not yet measured
  • 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 [482]

    The Results sections on patient and graft survival report no significant overall survival difference between recipients transplanted for NASH and those transplanted for non-NASH indications. This registry study supports the claim for NASH, but it does not establish the same result for the broader MASLD population. (LLM, conf=0.82)

    Experimental — accuracy not yet measured
  • In a large analysis of 68,950 adults undergoing first liver transplantation between 2002 and 2016 using the European Liver Transplant Registry database, individuals transplanted for MASH were more likely to have HCC, were older, and had a higher BMI.

    “In a large analysis of 68,950 adults undergoing fi rst liver transplantation between 2002 and 2016 using the European Liver Transplant Registry database, individuals transplanted for MASH were more likely to have HCC, were older, and had a higher BMI. 482”

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Authors
Haldar, D., Kern, B., Hodson, J., Armstrong, M. J., Adam, R., Berlakovich, G., Fritz, J., Feurstein, B., Popp, W., Karam, V., Muiesan, P., O'Grady, J., Jamieson, N., Wigmore, S. J., Pirenne, J., Malek-Hosseini, S. A., Hidalgo, E., Tokat, Y., Paul, A., Pratschke, J., Bartels, M., Trunecka, P., Settmacher, U., Pinzani, M., Duvoux, C., Newsome, P. N., & Schneeberger, S.
Affiliations
  • University Hospitals Birmingham NHS Foundation Trust (GB)
  • Innsbruck Medical University (AT)
  • Medical University of Vienna (AT)
  • Université Paris-Sud (FR)
  • Cambridge University Hospitals NHS Foundation Trust (GB)
  • Edinburgh Royal Infirmary (GB)
  • Universitair Ziekenhuis Leuven (BE)
  • Leeds Teaching Hospitals NHS Trust (GB)
  • Istanbul Florence Nightingale Hospital (TR)
  • Essen University Hospital (DE)
  • Charité – Universitätsmedizin Berlin (DE)
  • University Hospital Leipzig (DE)
  • Jena University Hospital (DE)
  • Royal Free London NHS Foundation Trust (GB)
  • Centre Hospitalier Universitaire Henri-Mondor (FR)
Corresponding author
Newsome, Philip Noel
Venue
Journal of Hepatology
Publisher
Elsevier BV
Published
2019-08
Volume
71
Issue
2
Pages
313-322
ISSN
0168-8278 (ISSN-L)
OpenAlex
W2942642723
Cited by
313
References
36
Citations by year
2026: 21 · 2025: 27 · 2024: 49 · 2023: 57 · 2022: 51 · 2021: 61 · 2020: 35 · 2019: 12
FWCI
37.99
Type
journal article
Language
en
Open access
Locations
  • Journal of Hepatology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • University of Birmingham Research Portal (University of Birmingham) (acceptedVersion, cc-by)
  • Edinburgh Research Explorer (University of Edinburgh) (acceptedVersion, cc-by)
  • Lirias (KU Leuven) (submittedVersion, other-oa)
  • Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
  • UCL Discovery (University College London) (submittedVersion)
  • Florence Research (University of Florence) (submittedVersion)
Funders
  • NIHR Birmingham Biomedical Research Centre (BRC-1215-20009)
  • University Hospitals Birmingham NHS Foundation Trust
  • University of Birmingham
  • Wellcome Trust (108741/Z/15/Z)
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
liver transplantation, nonalcoholic steatohepatitis, end-stage liver disease, allograft survival, hepatocellular carcinoma, prognostic factors, body mass index, MELD score, recipient age, post-transplant mortality, infectious complications, European Liver Transplant Registry, metabolic risk factors, obesity, underweight
MeSH terms
Adult, Age Factors, Europe, Female, Graft Survival, Carcinoma, Hepatocellular, Humans, Liver Neoplasms, Male, Middle Aged, Prospective Studies, Registries, Retrospective Studies, Risk Factors, Tissue Donors, Body Mass Index, Liver Transplantation, Treatment Outcome, End Stage Liver Disease, Non-alcoholic Fatty Liver Disease

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