Prognosis after hepatic resection of patients with hepatocellular carcinoma related to non-alcoholic fatty liver disease: meta-analysis

Jia-Yong Su; Zhu-Jian Deng; Yu-Xian Teng; Ye Xin Koh; Wan-Guang Zhang; Ming-Hua Zheng; Si Xie; Rong-Rui Huo; Chao-Jing Chen; Liang Ma; Jian-Hong Zhong

doi:10.1093/bjsopen/zrac167

. 2023 Feb 20;7(1):zrac167. doi: 10.1093/bjsopen/zrac167

Prognosis after hepatic resection of patients with hepatocellular carcinoma related to non-alcoholic fatty liver disease: meta-analysis

Jia-Yong Su ¹, Zhu-Jian Deng ², Yu-Xian Teng ³, Ye Xin Koh ⁴, Wan-Guang Zhang ⁵, Ming-Hua Zheng ⁶, Si Xie ⁷, Rong-Rui Huo ⁸, Chao-Jing Chen ⁹, Liang Ma ¹⁰, Jian-Hong Zhong ^11,^12,^✉

PMCID: PMC9939291 PMID: 36802244

Abstract

Background

Whether the safety and efficacy of hepatic resection differ between patients whose hepatocellular carcinoma (HCC) is related to non-alcoholic fatty liver disease (NAFLD) or has other aetiologies is unknown. A systematic review was performed to explore potential differences between such conditions.

Methods

PubMed, EMBASE, Web of Science, and Cochrane Library were systematically searched for relevant studies that reported hazard ratios (HRs) for overall and recurrence-free survival between patients with NAFLD-related HCC or HCC of other aetiologies.

Results

The meta-analysis involved 17 retrospective studies involving 2470 patients (21.5 per cent) with NAFLD-related HCC and 9007 (78.5 per cent) with HCC of other aetiologies. Patients with NAFLD-related HCC were older and had higher body mass index (BMI), but were less likely to have cirrhosis (50.4 per cent versus 64.0 per cent, P < 0.001). The two groups suffered similar rates of perioperative complications and mortality. Patients with NAFLD-related HCC had slightly higher overall survival (HR 0.87, 95 per cent c.i. 0.75 to 1.02) and recurrence-free survival (HR 0.93, 95 per cent c.i. 0.84 to 1.02) than those with HCC of other aetiologies. In the various subgroup analyses, the only significant finding was that Asian patients with NAFLD-related HCC had significantly better overall survival (HR 0.82, 95 per cent c.i. 0.71 to 0.95) and recurrence-free survival (HR 0.88, 95 per cent c.i. 0.79 to 0.98) than Asian patients with HCC of other aetiologies.

Conclusion

The available evidence suggests that patients with NAFLD-related HCC have similar perioperative complications and mortality, but potentially longer overall and recurrence-free survival, compared with those with HCC of other aetiologies. Tailored surveillance strategies should be developed for patients with NAFLD without cirrhosis.

Patients with non-alcoholic fatty liver disease (NAFLD)-related hepatocellular carcinoma (HCC) have similar perioperative complications and mortality compared with those with HCC of other aetiologies. Patients with NAFLD-related HCC have potentially higher overall and recurrence-free survival than those with HCC of other aetiologies.

Introduction

Hepatic resection is the only curative treatment for patients with hepatocellular carcinoma (HCC)^1–4. The main causes of HCC are chronic alcohol abuse and chronic infection with hepatitis B virus (HBV) or hepatitis C virus (HCV). The incidence of viral hepatitis-related HCC has decreased in recent years with the emergence and popularization of anti-hepatitis vaccines and antiviral drugs^5,6. Over the past decade, an increasingly prevalent risk factor for HCC in many countries is non-alcoholic fatty liver disease (NAFLD)^7,8. NAFLD refers to a spectrum of liver damage ranging from simple steatosis to non-alcoholic steatohepatitis (NASH), then fibrosis and cirrhosis, and finally to hepatocarcinogenesis. Although the annual incidence of HCC is lower among NAFLD patients than among those infected with HBV or HCV, 25 per cent of the global population is estimated to have NAFLD—with even higher prevalence in high-income areas^9,10—and the prevalence of NAFLD and NAFLD-related HCC is increasing in various countries^11–14. These considerations highlight the importance of preventing and treating NAFLD-related HCC.

Increasing evidence indicates that the pathogenesis and clinical manifestations of NAFLD-related HCC differ from those of HCC with other aetiologies. In addition, diabetes mellitus and obesity promote the progression of NAFLD to HCC^15,16. It is not clear whether these differences translate into a different prognosis after hepatic resection. Two meta-analyses have evaluated the safety and prognosis of hepatic resection for treating NAFLD-related HCC^17,18, but they included relatively few original studies, and several relevant studies have been published since then^19–22. Moreover, the meta-analyses were less rigorous in their inclusion criteria, such that some patients in the observation group did not meet diagnostic standards for NAFLD-related HCC^23–28, and some patients received palliative treatment instead of resection^29–33. Therefore, it was important to conduct an updated systematic review and meta-analysis of relevant clinical studies to compare prognosis after resection between patients with NAFLD-related HCC and patients with HCC of other aetiologies. This updated systematic review aims to provide a reference for selecting treatment for patients with NAFLD-related HCC.

Methods

This systematic review and meta-analysis was performed according to the guidelines of MOOSE ('Meta-analysis Of Observational Studies in Epidemiology’)³⁴ and PRISMA (Appendix S1). This was a systematic review pooling published data, so no ethical approval was required; since this study incorporated only previously published literature, approval from the local ethics committee to perform the research and informed consent from the patients in the included studies were not obtained.

Inclusion and exclusion criteria

In this review, patients with NAFLD-related HCC were grouped together with patients whose HCC was related to metabolic-associated fatty liver disease (MAFLD), which is the term recently proposed to replace NAFLD. MAFLD has been defined as chronic disease involving metabolic dysfunction that leads to accumulation of fat in the liver, such that fat mass accounts for greater than 5 per cent of total liver mass³⁵. Patients in the present review were diagnosed with MAFLD if they had hepatic steatosis as well as one of the following: overweight/obesity, defined as a body mass index (BMI) greater than or equal to 23 kg/m²; type 2 diabetes; or other evidence of metabolic disorder^35–38. Although MAFLD is closely linked to these metabolic disorders³⁹, its epidemiology is quite similar to that of NAFLD⁴⁰, so we grouped together data for HCC patients with either NAFLD or MAFLD.

The inclusion criteria, structured according to participants, interventions, comparisons, and outcomes (PICO) were as follows: adult HCC patients without geographical or aetiological limitations; patients who underwent hepatic resection, including laparotomy or laparoscopic surgery; patients who could be assigned to either a group with HCC related to NAFLD or MAFLD, or a group with HCC of other aetiologies; studies reporting data on overall survival (OS) and/or recurrence-free survival (RFS) as outcomes; and studies with a cohort or case-control design. Randomized clinical trials were not included.

Exclusion criteria were as follows: the study was a case report, review, or meta-analysis; patients received other therapies for HCC, such as radiofrequency ablation, sorafenib, lenvatinib, or other first-line therapies; or patients had other malignancies in addition to HCC. When multiple studies involved overlapping patient populations, only the largest study was included.

Data sources and literature search strategy

PubMed, EMBASE, Scopus, and Cochrane Library databases were systematically searched. Since NAFLD was first proposed in 1980, the database search time was set as 1 January 1980 to 25 June 2022, and the language of publication was limited to English. Search terms were: HCC, hepatoma, liver neoplasm, NAFLD, MAFLD, NASH, surgery, and survival. For example, the search string for the PubMed database was ‘(hepatocellular carcinoma OR liver neoplasm) AND (non-alcoholic fatty liver disease OR NAFLD OR nonalcoholic steatohepatitis OR NASH OR metabolic associated fatty liver disease OR MAFLD) AND (surgery OR resection OR hepatectomy) AND survival’.

Literature screening and data extraction

Two researchers (J.-Y.S. and Z.-J.D.) independently searched and screened the literature, then extracted relevant data from the included studies. Inconsistencies in the data were resolved through discussion with a third researcher (J.-H.Z.). The literature was screened based on titles, abstracts, and, when necessary, the full text. The following data were extracted from included studies: name of first author, publication year, country, inclusion interval, sample size, HCC aetiology and rate in the control group, average or median age of subjects, BMI, rate of cirrhosis, tumour stage, perioperative mortality, incidence of complications, OS, and RFS. For raw data that were not available, efforts were made to contact the corresponding author.

Outcomes

The primary outcome was the comparison of post-hepatectomy OS between patients with NAFLD- or MAFLD-related HCC (observation group) and patients with HCC with other aetiologies (control group). OS was defined as the time between the day of hepatectomy and the patient’s all-cause death or the end of follow-up. The secondary outcomes included RFS, perioperative mortality, and complication rates. RFS was defined as the time from the day of hepatectomy to the time of HCC recurrence or death, with the first HCC occurrence considered the primary event. Perioperative mortality was defined as death within 30 or 90 days after hepatectomy. Complications were defined as ‘major’ if they were graded as 3a or above according to the Clavien–Dindo classification system⁴¹. Other aetiologies of HCC included: viral hepatitis, related to HBV or HCV infection; alcoholic cirrhosis; and cryptogenic cirrhosis.

Evaluation of study quality

Two researchers (J.-Y.S. and Z.-J.D.) independently evaluated the quality of the included studies using the Newcastle–Ottawa scale (NOS) for quality assessment (Appendix S2)⁴². The scale includes eight multiple-choice questions that relate to patient selection, comparisons, and outcomes. Studies were assigned up to nine stars; those receiving at least seven stars were considered of good quality, while those receiving four to six stars were considered of fair quality. Inconsistencies were resolved through discussion with a third researcher (J.-H.Z.).

Statistical analysis

Continuous data were expressed as mean ± standard deviation if they showed a normal distribution, or as median (interquartile range) if they showed a skewed distribution. OS and RFS in both groups were assessed by combining log-transformed hazard ratios (HRs) and corresponding 95 per cent confidence intervals using an inverse variance, random-effects model. HRs and 95 per cent confidence intervals were extracted directly from the included literature; if these data were not reported, they were estimated indirectly using Parmar’s method⁴³.

Statistical heterogeneity was assessed using Higgins’ I² statistic and Cochran’s Q test⁴⁴. The I² gives a percentage representing the magnitude of heterogeneity between groups. A percentage of 25 per cent was taken to indicate low heterogeneity, a percentage of 50 per cent was taken to indicate moderate heterogeneity, and a percentage of 75 per cent was taken to indicate high heterogeneity. Publication bias was assessed using Egger’s and Begg’s regression analysis of funnel plots⁴⁵. Subgroup analysis was performed based on geographical region where studies were performed, or based on HCC aetiology. Sensitivity analysis was performed in which individual studies were omitted and the meta-analysis was repeated. Median OS and RFS at 1, 3, and 5 years were estimated with bubble charts, where the size of each bubble represented the sample size of the given study³. Meta-analyses were performed using RevMan (version 5.4.0) and R (version 3.5.0; R Foundation; http://cran.rproject.org). All statistical tests were two-sided, and differences associated with P < 0.050 were considered statistically significant.

Results

Literature search results

A total of 2492 publications were retrieved from relevant databases based on the inclusion and exclusion criteria. Thirteen publications were excluded because they included patients without steatosis^23–28 or who received palliative treatment^29–33, because the studies did not report survival data⁴⁶ or because of repeat publication⁴⁷. In the end, 17 retrospective studies were included (Fig. 1)^{19–22,48–60}.

Fig. 1 — PRISMA diagram showing selection of articles for meta-analysis

MAFLD, metabolic-associated fatty liver disease; NAFLD, non-alcoholic fatty liver disease; NASH, non-alcoholic steatohepatitis.

Characteristics of included studies and patients

Basic characteristics of the literature included in this systematic review are shown in Table 1. The studies covered 28 years (1991–2019). Of the 17 studies, 10 applied standard definitions of NAFLD^{21,48–51,54,55,57–59}, 4 applied standard definitions of MAFLD^19,20,22,60, 2 applied standard definitions of steatosis^53,56, and 1 applied a standard definition of NASH⁵². Patients in all studies except one underwent hepatectomy; those in the study applying a standard definition of NASH⁵² underwent liver transplantation, hepatectomy, and radiofrequency ablation, all of which are radical treatments. All studies had a retrospective cohort design and most (94.1 per cent) showed high quality except one with fair quality⁵³ (Table S1).

Table 1.

Baseline characteristics of patients with hepatocellular carcinoma associated with non-alcoholic fatty liver disease or metabolic-associated fatty liver disease and patients with hepatocellular carcinoma of other aetiologies

Study	Country/region and inclusion interval	Aetiology	Sample size	Age (years)*	BMI (kg/m²)*	Cirrhosis	Macrovascular invasion	Complications (Clavien–Dindo >3a)	90-day mortality
Liu 2022¹⁹	China, 2014–2018	MAFLD	67	58.8	≥23: 42 (62.7)	34 (50.7)	7 (10.4)	3 (4.5)	0 (0)
		MAFLD/HBV	176	49.4	≥23: 166 (94.3)	120 (68.2)	21 (11.9)	18 (10.2)	0 (0)
		HBV	1082	48.9	≥23: 360 (33.3)	771 (71.3)	197 (18.2)	85 (7.9)	2 (0.2)
Conci 2022²⁰	Italy, 2008–2018	MAFLD	264	71	27.8	101 (38.3)	31 (11.7)	19 (7.2)	11 (4.2)
		HBV	205	68	24.0	122 (59.5)	53 (25.9)	17 (8.3)	5 (2.4)
		HCV	671	72	24.0	491 (73.2)	94 (14.0)	62 (9.2)	21 (3.1)
		Alcohol	175	70	25.0	115 (65.7)	14 (8.0)	11 (6.3)	3 (1.7)
Jung 2021²¹	South Korea, 2005–2015	NAFLD	32	61	26.6	5 (16)	1 (3.1)	2 (6)	2 (6)
		NAFLD/HBV	194	55	24.7	126 (65)	13 (6.7)	15 (8)	3 (2)
		HBV	200	54	23.2	110 (55)	14 (7.0)	11 (6)	5 (3)
Lin 2021²²	Taiwan, 2010–2019	MAFLD/HBV	369	56.2	26.7	181 (49.1)	0 (0)	–	–
Lin 2021²²	Taiwan, 2010–2019	HBV	443	56.2	23.9	229 (51.7)	0 (0)	–	–
Kimura 2017⁴⁸	Japan, 1996–2012	NAFLD	30	71	25.0	8 (27)	7 (23.3)	–	–
		Alcohol	31	69	22.4	18 (58)	11 (35.5)	–	–
		Cryptogenic	16	75	22.6	4 (25)	12 (75.0)	–	–
Koh 2019⁴⁹	Singapore, 2000–2015	NAFLD	152	69	25.4	52 (34.2)	–	24 (16.2)	3 (1.99)
Koh 2019⁴⁹	Singapore, 2000–2015	Non-NAFLD	844	63	25.0	429 (51.1)	–	68 (8.1)	21 (2.46)
Mikuriya 2015⁵⁰	Japan, 1998–2011	NAFLD	21	69.3	–	–	–	–	–
Mikuriya 2015⁵⁰	Japan, 1998–2011	HCV	645	66.3	–	–	–	–	–
Pais 2017⁵¹	France, 1995–2014	NAFLD	39	70	27.6	9 (23.1)	17 (43.6)	–	–
Pais 2017⁵¹	France, 1995–2014	Non-NAFLD	284	58	24.4	182 (64.1)	122 (43.0)	–	–
Reddy 2012⁵²	USA, 2000–2010	NASH	52	65	31.3	–	3 (5.8)	–	–
Reddy 2012⁵²	USA, 2000–2010	HCV/alcohol	162	58	28.7	–	14 (8.6)	–	–
Su 2015⁵³	Taiwan, 1991–2006	Steatosis	74	60.5	25.1	43 (58.1)	3 (4.1)	–	–
Su 2015⁵³	Taiwan, 1991–2006	No steatosis	114	62.5	23.0	68 (59.6)	4 (3.5)	–	–
Wakai 2011⁵⁴	Japan, 1990–2007	NAFLD	17	>65: 13 (76.5)	>25: 11 (64.7)	9 (52.9)	7 (41.2)	All: 10 (58.8)	2 (11.8)
		HBV	61	>65: 14 (23.0)	>25: 12 (19.7)	39 (63.9)	27 (44.3)	All: 17 (27.9)	2 (3.3)
		HCV	147	>65: 84 (57.1)	>25: 24 (16.3)	84 (57.1)	41 (27.9)	All: 45 (30.6)	1 (0.7)
Wong 2017⁵⁵	USA, 1991–2011	NAFLD	178	–	–	–	–	–	–
		HCV	413	–	–	–	–	–	–
		HBV	215	–	–	–	–	–	–
		Alcohol	60	–	–	–	–	–	–
Wu 2011⁵⁶	Taiwan, 1999–2005	Steatosis	355	57.5	25.2	208 (58.6)	111 (31.3)	All: 106 (29.9)	16 (4.5)
Wu 2011⁵⁶	Taiwan, 1999–2005	No steatosis	693	55.7	23.6	396 (57.1)	277 (40.0)	All: 192 (27.7)	34 (4.9)
Yang 2020⁵⁷	China, 2003–2014	NAFLD	96	57.3	-	29 (30.2)	10 (10.4)	8 (9.4)	1 (1.0)
Yang 2020⁵⁷	China, 2003–2014	HBV	1387	50.0	-	1006 (72.5)	195 (14.1)	140 (10.1)	19 (1.4)
Yoon 2020⁵⁸	South Korea, 2009–2013	NAFLD/HBV	196	55.0	24.1	85 (43.4)	–	–	–
Yoon 2020⁵⁸	South Korea, 2009–2013	HBV	142	57.0	22.5	54 (38.0)	–	–	–
D'Silva 2022⁵⁹	South Korea, 2004–2018	NAFLD	54	65.8	>25: 38 (70.4)	33 (61.1)	–	4 (7.4)	–
D'Silva 2022⁵⁹	South Korea, 2004–2018	HBV	589	56.4	>25: 239 (40.6)	364 (61.8)	–	72 (12.2)	–
Xiong 2022⁶⁰	China, 2015–2018	MAFLD/HBV	104	57.0	24.5	76 (73.1)	0 (0)	–	–
Xiong 2022⁶⁰	China, 2015–2018	HBV	428	57.0	22.2	324 (75.7)	0 (0)	–	–

Open in a new tab

Values are n (%) unless otherwise indicated. *Median or mean. BMI, body mass index; MAFLD, metabolic-associated fatty liver disease; HBV, hepatitis B virus; HCV, hepatitis C virus; Alcohol, alcoholic cirrhosis; NAFLD, non-alcoholic fatty liver disease; Cryptogenic, cryptogenic cirrhosis.

The 17 studies included 11 477 patients, including 2470 (21.5 per cent) with NAFLD-related HCC and 9007 (78.5 per cent) with HCC of other aetiologies (Table 1). The prevalence of NALFD-related HCC in Asian patients was significantly higher compared with that in European and US patients (P = 0.006; Fig. S1). Compared with patients with HCC of other aetiologies, those with NAFLD-related HCC had a higher BMI, they were older in 11 studies^{19,21,49–52,54–57,59}, and they showed significantly lower cirrhosis rates in 11 studies^{19–22,48,49,51,53–55,57} of the 15 that reported cirrhosis rates^{19–22,48,49,51,53–60}. When cirrhosis rates were calculated across all patients pooled from the studies, prevalence was significantly lower in the observation group than in the control group (P < 0.001). Patients with HCC irrespective of aetiology from Asia and those from the USA and Europe had a similar proportion of cirrhosis (P = 0.212; Fig. 2a). Among patients with NAFLD-related HCC, patients from Asia had a significantly higher proportion of cirrhosis than those from the USA and Europe (P < 0.001; Fig. 2b). However, among patients with HCC of other aetiologies, US and European patients had a significantly higher proportion of cirrhosis than those from Asia (P < 0.001; Fig. 2c). Moreover, the proportion of cirrhosis among patients with NAFLD-related HCC was significantly lower than that among those with alcohol-, HBV-, or HCV-related HCC (all P < 0.001; Fig. 2d).

Fig. 2 — Proportion of patients with cirrhosis and hepatocellular carcinoma

a HCC irrespective of aetiology. b HCC related to NAFLD or MAFLD. c HCC of other aetiologies. d HCC related to different aetiologies. ALD, alcoholic cirrhosis disease; Cry, cryptogenic; HBV, hepatitis B virus; HCC, hepatocellular carcinoma; HCV, hepatitis C virus; MAFLD, metabolic-associated fatty liver disease; NAFLD, non-alcoholic fatty liver disease.

Perioperative complications and mortality

Eight studies reported the incidence of perioperative complications, which was higher in the observation group than in the control group in four studies^49,54,56,59, lower in the observation group in two studies^19,57, and similar between the observation and control groups in the other two studies^20,21. Pooling the patients across all eight studies showed that the rate of major complications was similar between the observation group (8.98 per cent, 93/1035) and control group (9.0 per cent, 466/5153; P = 1.000).

Seven studies reported perioperative mortality, which was higher in the observation group in three studies^20,21,54, but similar between the observation and control groups in the remaining four studies^19,49,56,57. When rates of perioperative mortality were calculated across all patients pooled from the studies, the rate was similar between the observation group (2.9 per cent, 35/1201) and control group (2.1 per cent, 116/5617; P = 0.083).

Overall survival

Data pooled from the 16 studies that reported OS^{19–22,48–50,52–60} showed that patients with NAFLD-related HCC had marginally higher OS than those with HCC of other aetiologies (HR 0.87, 95 per cent c.i. 0.75 to 1.02, P = 0.051; Fig. 3), as well as higher median OS rates at 1 year (94.5 per cent versus 90.0 per cent), 3 years (75.3 per cent versus 70.2 per cent), and 5 years (67.9 per cent versus 59.0 per cent; Fig. 4a). This difference became significant among the subset of studies involving Asian patients (P < 0.001; Fig. S2), but not among the subset of studies involving patients from the US and Europe (P = 0.934; Fig. S2).

Fig. 3 — Comparison of overall survival between patients with hepatocellular carcinoma related to non-alcoholic fatty liver disease or metabolic-associated fatty liver disease and patients with hepatocellular carcinoma of other aetiologies

HBV, hepatitis B virus; HCV, hepatitis C virus; MAFLD, metabolic-associated fatty liver disease; NAFLD, non-alcoholic fatty liver disease; NASH, non-alcoholic steatohepatitis.

Fig. 4 — Bubble plots of 1-, 3-, and 5-year survival of patients with hepatocellular carcinoma related to non-alcoholic fatty liver disease or metabolic-associated fatty liver disease and patients with hepatocellular carcinoma of other aetiologies

a Overall survival. b Recurrence-free survival. The size of each bubble represents the sample size of the given study NAFLD, non-alcoholic fatty liver disease.

In subgroup analyses based on HCC aetiology, patients with NAFLD-related HCC showed similar OS to those with HCC related to HBV or HCV infection (P = 0.134; Fig. S3) and those with HCC related to alcoholic or cryptogenic cirrhosis (P = 0.413; Fig. S3). In contrast, the OS of patients with HCC related specifically to NAFLD, based on studies applying standard definitions of NAFLD^{21,48–51,54,55,57–59}, was significantly better than the OS of patients with HCC of other aetiologies (P = 0.012; Fig. S4).

Recurrence-free survival

Data pooled from the 16 studies that reported RFS^{19–22,48–54,56–60} showed that patients with NAFLD-related HCC had marginally better RFS than patients with HCC of other aetiologies (HR 0.93, 95 per cent c.i. 0.85 to 1.01, P = 0.128; Fig. 5), as well as higher median RFS rates at 1 year (80.0 per cent versus 72.0 per cent), 3 years (52.1 per cent versus 45.3 per cent), and 5 years (41.6 per cent versus 38.0 per cent; Fig. 4b). This difference became significant among the subset of studies involving Asian patients (P = 0.02; Fig. S5), but not among the subset of studies involving patients from the US and Europe (P = 0.466; Fig. S5).

Fig. 5 — Comparison of recurrence-free survival between patients with hepatocellular carcinoma related to non-alcoholic fatty liver disease or metabolic-associated fatty liver disease and patients with hepatocellular carcinoma of other aetiologies

HBV, hepatitis B virus; HCV, hepatitis C virus; MAFLD, metabolic-associated fatty liver disease; NAFLD, non-alcoholic fatty liver disease; NASH, non-alcoholic steatohepatitis.

In subgroup analyses based on HCC aetiology, patients with NAFLD-related HCC showed similar RFS to those with HCC related to HBV or HCV infection (P = 0.283; Fig. S6) and those with HCC related to alcoholic or cryptogenic cirrhosis (P = 0.327; Fig. S6). A similar result was found when considering the RFS of patients with HCC related specifically to NAFLD, based on studies applying standard definitions of NAFLD^{21,48–51,54,55,57–59} (P = 0.464; Fig. S7).

Sensitivity analysis

None of the meta-analysis findings changed after the exclusion of patients who underwent liver transplantation or radiofrequency ablation⁵². Excluding each study one by one altered the meta-analysis of OS in the case of Conci 2022²⁰ (MAFLD versus HBV), Jung 2021²¹ (MAFLD versus HBV), and Su 2015⁵³ (steatosis versus without) (Fig. S8). Moreover, excluding each study one by one altered the meta-analysis of RFS in the case of Liu 2022¹⁹ (MAFLD versus HBV), Pais 2017⁵¹ (NAFLD versus HBV), Pais 2017⁵¹ (NAFLD versus HCV), and Su 2015⁵³ (steatosis versus without) (Fig. S8).

Publication bias

No significant publication bias was found in funnel plots for OS (P = 0.487; Fig. S9) or RFS (P = 0.672; Fig. S9).

Discussion

As NAFLD/MAFLD becomes more prevalent, treating HCC related to NAFLD/MAFLD becomes relevant. In this context, it may help clinicians and patients in their treatment decisions to know whether post-hepatectomy outcomes differ significantly between patients with NAFLD- or MAFLD-related HCC and patients with HCC of other aetiologies. The present meta-analysis of 11 477 cases from 17 studies suggests that the two groups of patients show similar rates of major perioperative complications, OS, and RFS after hepatic resection. However, when focusing on studies performed in Asia, significantly better OS and RFS for patients with NAFLD- or MAFLD-related HCC than for those with HCC of other aetiologies were found.

The finding of similar OS and RFS between the two groups of patients contrasts with the significantly higher survival reported for patients with NAFLD- or MAFLD-related HCC in two previous meta-analyses involving 7226¹⁷ and 5579 patients respectively¹⁸. The present results may be more reliable because the sample is substantially larger (11 477 patients) and the inclusion criteria are more stringent. All patients in the analysis underwent hepatectomy, and all patients in the observation group fulfilled standard diagnostic criteria for NAFLD- or MAFLD-related HCC. Nevertheless, the meta-analyses showed substantial statistical heterogeneity, especially the meta-analysis of OS. This may reflect that patients were enrolled over a 28-year interval, different medical centres may define fatty liver in different ways, and the patient samples in individual studies differed substantially in the rates of cirrhosis. The influence of these factors on the meta-analyses could not be assessed because of the lack of patient-level data.

The patients with NAFLD- or MAFLD-related HCC in this review were older and more likely to have diabetes, obesity, hyperlipidaemia, or other metabolic disorders than the patients with HCC of other aetiologies. Nevertheless, the two groups showed similar rates of major perioperative complications (8.98 per cent versus 9.0 per cent, P = 1.000) and mortality (2.9 per cent versus 2.1 per cent, P = 0.083). These results likely reflect the substantial improvement in surgical techniques and perioperative management of hepatectomy. A systematic review of 14 808 patients who underwent hepatectomy for intermediate or advanced HCC found a low perioperative mortality of 2.7 per cent⁶¹.

One explanation for the finding, across all studies, that patients with NAFLD- or MAFLD-related HCC have slightly better OS or RFS than patients with HCC of other aetiologies is the fact that the first group of patients showed a significantly lower prevalence of cirrhosis (50.4 per cent versus 64.0 per cent, P < 0.001). Cirrhosis is an independent risk factor for all-cause mortality in patients with NAFLD, NASH, or HCC. The finding that OS and RFS were significantly higher among patients with NAFLD- or MAFLD-related HCC than among those with HCC of other aetiologies in Asia but not in Europe and the USA may reflect regional differences in HCC aetiology and tumour characteristics^62,63. For example, hepatectomy is often used in Asia to treat HCC patients for whom surgery is not recommended in the USA or Europe^2,64–66. Finally, the results may also reflect the relatively small number of patients from Europe and the USA in the meta-analysis.

Many of the patients in five studies^29–33 of a previous meta-analysis¹⁷ not included in the present one received transarterial chemoembolization, radiotherapy, chemotherapy, or best supportive care instead of hepatectomy. All five of those studies reported similar OS between patients with NAFLD- or NASH-related HCC and patients with HCC related to viral hepatitis or alcohol (Table S2). However, other studies found that lenvatinib treatment may lead to better OS, while immune checkpoint inhibitors may lead to worse OS when treating NAFLD-related HCC compared with HCC of other aetiologies^67,68. In addition to hepatectomy, liver transplantation and radiofrequency ablation can be applied as radical therapies against HCC. One meta-analysis reported similar post-transplantation OS between patients with NASH-related HCC or HCC of other aetiologies⁶⁹. Two cohort studies found similar post-ablation OS between patients with NAFLD-related HCC and patients with HCC of other aetiologies^55,70.

Half of the patients with NAFLD-related HCC had no cirrhosis. This rate was as high as 63.7 per cent in the US and European populations. However, the proportion of patients without cirrhosis among those with alcohol-, HBV-, or HCV-related HCC was only 35.4 per cent, 33.5 per cent, and 29.7 per cent respectively. Therefore, patients with NAFLD without cirrhosis still need regular surveillance for HCC. This finding based on patients with HCC after hepatectomy was consistent with a previous meta-analysis that included patients with NAFLD-related HCC who underwent curative and palliative treatment strategies⁷¹.

Despite the stricter inclusion criteria, the present meta-analysis involved a substantially larger sample than previous ones. In addition, the present meta-analysis included MAFLD-related HCC and took into account the prevalence of cirrhosis, incidence of major perioperative complications, and mortality. However, it was limited by the fact that the included studies had a retrospective cohort design, with no access to patient-level data. Most patients in the meta-analysis came from Asia, which may reduce the generalizability of the results to other regions. Finally, heterogeneity among included studies was large.

This study systematically reviewed post-hepatectomy outcomes of patients with HCC of different aetiologies. The analysis suggests that patients with NAFLD- or MAFLD-related HCC show similar major perioperative complications, mortality, OS, and RFS compared with patients with HCC of other aetiologies. However, Asian patients may have better survival if their HCC is related to NAFLD or MAFLD. The surveillance for HCC in NAFLD patients without cirrhosis is equally important as surveillance for HCC in NAFLD patients with cirrhosis.

Supplementary Material

zrac167_Supplementary_Data

Click here for additional data file.^{(2.5MB, docx)}

Acknowledgements

We thank Dr Yoon Bin Jung (Yonsei University School of Medicine, South Korea) for providing some original data.

The corresponding author had full access to all the data in the study and had final responsibility for the decision to submit for publication.

Author contributions: J.-H.Z. conceived the study; Z.-J.D., J.-Y.S., and S.X. collected and analysed the data; Y.-X.T., R.-R.H., C.-J.C., M.-H.Z. and J.-H.Z. analysed the data; J.-Y.S. and J.-H.Z. drafted the manuscript; L.M., Y.X.K., W.-G.Z., and J.-H.Z. revised the manuscript; all authors read and approved the final version to be published.

Guarantor of the article: J.-H.Z.

Contributor Information

Jia-Yong Su, Hepatobiliary Surgery Department, Guangxi Medical University Cancer Hospital, Nanning, China.

Zhu-Jian Deng, Hepatobiliary Surgery Department, Guangxi Medical University Cancer Hospital, Nanning, China.

Yu-Xian Teng, Hepatobiliary Surgery Department, Guangxi Medical University Cancer Hospital, Nanning, China.

Ye Xin Koh, Department of Hepatopancreatobiliary and Transplant Surgery, Singapore General Hospital, Singapore.

Wan-Guang Zhang, Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China.

Ming-Hua Zheng, NAFLD Research Center, Department of Hepatology, the First Affiliated Hospital of Wenzhou Medical University, Wenzhou, China.

Si Xie, Hepatobiliary Surgery Department, Guangxi Medical University Cancer Hospital, Nanning, China.

Rong-Rui Huo, Hepatobiliary Surgery Department, Guangxi Medical University Cancer Hospital, Nanning, China.

Chao-Jing Chen, Hepatobiliary Surgery Department, Guangxi Medical University Cancer Hospital, Nanning, China.

Liang Ma, Hepatobiliary Surgery Department, Guangxi Medical University Cancer Hospital, Nanning, China.

Jian-Hong Zhong, Hepatobiliary Surgery Department, Guangxi Medical University Cancer Hospital, Nanning, China; Key Laboratory of Early Prevention and Treatment for Regional High Frequency Tumor (Guangxi Medical University), Ministry of Education; Guangxi Key Laboratory of Early Prevention and Treatment for Regional High Frequency Tumor, Nanning, China.

Funding

This work was supported by the Specific Research Project of Guangxi for Research Bases and Talents (GuiKe AD22035057), the National Natural Science Foundation of China (82060510 and 82260569), the Guangxi Undergraduate Training Program for Innovation and Entrepreneurship (X202210598347), and the Innovation Project of Guangxi Graduate Education (YCSW2022226).

The funders of the study had no role in study design, data collection, data analysis, data interpretation, or writing of the report.

Disclosure

The authors declare no conflict of interest.

Supplementary material

Supplementary material is available at BJS Open online.

Data availability

All data are in the manuscript. Supplementary material for this article is available online.

References

1. Galle PR, Forner A, Llovet JM, Mazzaferro V, Piscaglia F, Raoul J-Let al. EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 2018;69:182–236 [DOI] [PubMed] [Google Scholar]
2. Zhong JH, Ke Y, Wang YY, Li LQ. Liver resection for patients with hepatocellular carcinoma and macrovascular invasion, multiple tumours, or portal hypertension. Gut 2015;64:520–521 [DOI] [PubMed] [Google Scholar]
3. Yuan BH, Zhu YK, Zou XM, Zhou HD, Li RH, Zhong JH. Repeat hepatic resection versus ablation for patients with recurrent hepatocellular carcinoma: a systematic review. BJS Open 2022;6:zrac036 [DOI] [PMC free article] [PubMed] [Google Scholar]
4. Zhong JH, Xing BC, Zhang WG, Chan AW, Chong CCN, Serenari Met al. Repeat hepatic resection versus radiofrequency ablation for recurrent hepatocellular carcinoma: a retrospective multicentre study. Br J Surg 2022;109:71–78 [DOI] [PubMed] [Google Scholar]
5. Knudsen ES, Gopal P, Singal AG. The changing landscape of hepatocellular carcinoma: etiology, genetics, and therapy. Am J Pathol 2014;184:574–583 [DOI] [PMC free article] [PubMed] [Google Scholar]
6. Wang XY, Huang JM, Lu XM, Harrison TJ, Liu HB, Jia HHet al. Changing risk factors for hepatocellular carcinoma in hyperendemic regions in the era of universal hepatitis B vaccination. Cancer Epidemiol 2020;67:101775 [DOI] [PubMed] [Google Scholar]
7. Tateishi R, Okanoue T, Fujiwara N, Okita K, Kiyosawa K, Omata Met al. Clinical characteristics, treatment, and prognosis of non-B, non-C hepatocellular carcinoma: a large retrospective multicenter cohort study. J Gastroenterol 2015;50:350–360 [DOI] [PMC free article] [PubMed] [Google Scholar]
8. Younossi ZM, Koenig AB, 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 [DOI] [PubMed] [Google Scholar]
9. Eguchi Y, Wong G, Lee IH, Akhtar O, Lopes R, Sumida Y. Hepatocellular carcinoma and other complications of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in Japan: a structured review of published works. Hepatol Res 2021;51:19–30 [DOI] [PubMed] [Google Scholar]
10. Huang DQ, El-Serag HB, Loomba R. Global epidemiology of NAFLD-related HCC: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol 2021;18:223–238 [DOI] [PMC free article] [PubMed] [Google Scholar]
11. Estes C, Anstee QM, Arias-Loste MT, Bantel H, Bellentani S, Caballeria Jet al. Modeling NAFLD disease burden in China, France, Germany, Italy, Japan, Spain, United Kingdom, and United States for the period 2016–2030. J Hepatol 2018;69:896–904 [DOI] [PubMed] [Google Scholar]
12. Orci LA, Sanduzzi-Zamparelli M, Caballol B, Sapena V, Colucci N, Torres Fet al. Incidence of hepatocellular carcinoma in patients with nonalcoholic fatty liver disease: a systematic review, meta-analysis, and meta-regression. Clin Gastroenterol Hepatol 2022;20:283–292.e10 [DOI] [PubMed] [Google Scholar]
13. Le MH, Yeo YH, Li X, Li J, Zou B, Wu Yet al. 2019 Global NAFLD prevalence: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 2022;20:2809–2817.e28 [DOI] [PubMed] [Google Scholar]
14. Teng YX, Liu HT, Deng ZJ, Su JY, Lu YH, Zhong JH. Prevalence of MAFLD-related hepatocellular carcinoma. EJMO 2022;6:190–191 [Google Scholar]
15. Chen J, Song S, Li X, Bian D, Wu X. Association of metabolic traits with occurrence of nonalcoholic fatty liver disease-related hepatocellular carcinoma: a systematic review and meta-analysis of longitudinal cohort studies. Saudi J Gastroenterol 2022;28:92–100 [DOI] [PMC free article] [PubMed] [Google Scholar]
16. Rios RS, Zheng KI, Zheng MH. Non-alcoholic steatohepatitis and risk of hepatocellular carcinoma. Chin Med J (Engl) 2021;134:2911–2921 [DOI] [PMC free article] [PubMed] [Google Scholar]
17. Molinari M, Kaltenmeier C, Samra PB, Liu H, Wessel C, Lou Klem Met al. Hepatic resection for hepatocellular carcinoma in nonalcoholic fatty liver disease: a systematic review and meta-analysis of 7226 patients. Ann Surg Open 2021;2:e065. [DOI] [PMC free article] [PubMed] [Google Scholar]
18. Chin KM, Prieto M, Cheong CK, Di Martino M, Ielpo B, Goh BKPet al. Outcomes after curative therapy for hepatocellular carcinoma in patients with non-alcoholic fatty liver disease: a meta-analysis and review of current literature. HPB (Oxford) 2021;23:1164–1174 [DOI] [PubMed] [Google Scholar]
19. Liu L, Xie S, Teng YX, Deng ZJ, Chen K, Liu HTet al. Outcomes of hepatectomy for metabolic dysfunction-associated fatty liver disease or chronic hepatitis B-related HCC. Front Oncol 2022;11:783339 [DOI] [PMC free article] [PubMed] [Google Scholar]
20. Conci S, Cipriani F, Donadon M, Marchitelli I, Ardito F, Famularo Set al. Hepatectomy for metabolic associated fatty liver disease (MAFLD) related HCC: propensity case-matched analysis with viral- and alcohol-related HCC. Eur J Surg Oncol 2022;48:103–112 [DOI] [PubMed] [Google Scholar]
21. Jung YB, Yoo JE, Han DH, Kim KS, Choi JS, Kim DYet al. Clinical and survival outcomes after hepatectomy in patients with non-alcoholic fatty liver and hepatitis B-related hepatocellular carcinoma. HPB (Oxford) 2021;23:1113–1122 [DOI] [PubMed] [Google Scholar]
22. Lin YP, Lin SH, Wang CC, Lin CC, Chen DW, Chuang CHet al. Impact of MAFLD on HBV-related stage 0/A hepatocellular carcinoma after curative resection. J Pers Med 2021;11:684. [DOI] [PMC free article] [PubMed] [Google Scholar]
23. Cauchy F, Zalinski S, Dokmak S, Fuks D, Farges O, Castera Let al. Surgical treatment of hepatocellular carcinoma associated with the metabolic syndrome. Br J Surg 2013;100:113–121 [DOI] [PubMed] [Google Scholar]
24. Ishizuka M, Kubota K, Kita J, Shimoda M, Kato M, Sawada T. Survival after surgery for hepatocellular carcinoma in relation to presence or absence of viral infection. Am J Surg 2013;206:187–193 [DOI] [PubMed] [Google Scholar]
25. Liang J, Ariizumi SI, Nakano M, Yamamoto M. Diabetes mellitus and/or nonalcoholic steatohepatitis-related hepatocellular carcinoma showed favorable surgical outcomes after hepatectomy. Anticancer Res 2019;39:5639–5643 [DOI] [PubMed] [Google Scholar]
26. Nishio T, Hatano E, Sakurai T, Taura K, Okuno M, Kasai Yet al. Impact of hepatic steatosis on disease-free survival in patients with non-B non-C hepatocellular carcinoma undergoing hepatic resection. Ann Surg Oncol 2015;22:2226–2234 [DOI] [PubMed] [Google Scholar]
27. Tian Y, Lyu H, He Y, Xia Y, Li J, Shen F. Comparison of hepatectomy for patients with metabolic syndrome-related HCC and HBV-related HCC. J Gastrointest Surg 2018;22:615–623 [DOI] [PubMed] [Google Scholar]
28. Vigano L, Conci S, Cescon M, Fava C, Capelli P, D'Errico Aet al. Liver resection for hepatocellular carcinoma in patients with metabolic syndrome: a multicenter matched analysis with HCV-related HCC. J Hepatol 2015;63:93–101 [DOI] [PubMed] [Google Scholar]
29. Lin BZ, Lin TJ, Lin CL, Liao LY, Chang TA, Lu BJet al. Differentiation of clinical patterns and survival outcomes of hepatocellular carcinoma on hepatitis B and nonalcoholic fatty liver disease. J Chin Med Assoc 2021;84:606–613 [DOI] [PubMed] [Google Scholar]
30. Piscaglia F, Svegliati-Baroni G, Barchetti A, Pecorelli A, Marinelli S, Tiribelli Cet al. Clinical patterns of hepatocellular carcinoma in nonalcoholic fatty liver disease: a multicenter prospective study. Hepatology 2016;63:827–838 [DOI] [PubMed] [Google Scholar]
31. Kumar R, Goh BG, Kam JW, Chang PE, Tan CK. Comparisons between non-alcoholic steatohepatitis and alcohol-related hepatocellular carcinoma. Clin Mol Hepatol 2020;26:196–208 [DOI] [PMC free article] [PubMed] [Google Scholar]
32. Weinmann A, Alt Y, Koch S, Nelles C, Duber C, Lang Het al. Treatment and survival of non-alcoholic steatohepatitis associated hepatocellular carcinoma. BMC Cancer 2015;15:210. [DOI] [PMC free article] [PubMed] [Google Scholar]
33. Tokushige K, Hashimoto E, Yatsuji S, Tobari M, Taniai M, Torii Net al. Prospective study of hepatocellular carcinoma in nonalcoholic steatohepatitis in comparison with hepatocellular carcinoma caused by chronic hepatitis C. J Gastroenterol 2010;45:960–967 [DOI] [PubMed] [Google Scholar]
34. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie Det al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA 2000;283:2008–2012 [DOI] [PubMed] [Google Scholar]
35. Eslam M, Newsome PN, Sarin SK, Anstee QM, Targher G, Romero-Gomez Met al. A new definition for metabolic dysfunction-associated fatty liver disease: an international expert consensus statement. J Hepatol 2020;73:202–209 [DOI] [PubMed] [Google Scholar]
36. Eslam M, Sarin SK, Wong VW, Fan JG, Kawaguchi T, Ahn SHet al. The Asian Pacific Association for the Study of the Liver clinical practice guidelines for the diagnosis and management of metabolic associated fatty liver disease. Hepatol Int 2020;14:889–919 [DOI] [PubMed] [Google Scholar]
37. Shiha G, Alswat K, Al Khatry M, Sharara AI, Ormeci N, Waked Iet al. Nomenclature and definition of metabolic-associated fatty liver disease: a consensus from the Middle East and north Africa. Lancet Gastroenterol Hepatol 2021;6:57–64 [DOI] [PubMed] [Google Scholar]
38. Chan WK, Tan SS, Chan SP, Lee YY, Tee HP, Mahadeva Set al. The Malaysian Society of Gastroenterology and hepatology consensus statement on metabolic dysfunction-associated fatty liver disease. J Gastroenterol Hepatol 2022;37:795–811 [DOI] [PMC free article] [PubMed] [Google Scholar]
39. Lim S, Kim JW, Targher G. Links between metabolic syndrome and metabolic dysfunction-associated fatty liver disease. Trends Endocrinol Metab 2021;32:500–514 [DOI] [PubMed] [Google Scholar]
40. Yu C, Wang M, Zheng S, Xia M, Yang H, Zhang Det al. Comparing the diagnostic criteria of MAFLD and NAFLD in the Chinese population: a population-based prospective cohort study. J Clin Transl Hepatol 2022;10:6–16 [DOI] [PMC free article] [PubMed] [Google Scholar]
41. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240:205–213 [DOI] [PMC free article] [PubMed] [Google Scholar]
42. Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos Met al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp (accessed 20 December 2021)
43. Parmar MKB, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med 1998;17:2815–2834 [DOI] [PubMed] [Google Scholar]
44. Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003;327:557–560 [DOI] [PMC free article] [PubMed] [Google Scholar]
45. Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315:629–634 [DOI] [PMC free article] [PubMed] [Google Scholar]
46. Salomao M, Yu WM, Brown RS Jr, Emond JC, Lefkowitch JH. Steatohepatitic hepatocellular carcinoma (SH-HCC): a distinctive histological variant of HCC in hepatitis C virus-related cirrhosis with associated NAFLD/NASH. Am J Surg Pathol 2010;34:1630–1636 [DOI] [PubMed] [Google Scholar]
47. D'Silva M, Na HY, Cho JY, Han HS, Yoon YS, Lee HWet al. Pathological prognostic factors for post-resection survival in patients with hepatocellular carcinoma associated with non-alcoholic fatty liver disease. Transl Cancer Res 2021;10:3345–3355 [DOI] [PMC free article] [PubMed] [Google Scholar]
48. Kimura T, Kobayashi A, Tanaka N, Sano K, Komatsu M, Fujimori Net al. Clinicopathological characteristics of non-B non-C hepatocellular carcinoma without past hepatitis B virus infection. Hepatol Res 2017;47:405–418 [DOI] [PubMed] [Google Scholar]
49. Koh YX, Tan HJ, Liew YX, Syn N, Teo JY, Lee SYet al. Liver resection for nonalcoholic fatty liver disease-associated hepatocellular carcinoma. J Am Coll Surg 2019;229:467–478.e1 [DOI] [PubMed] [Google Scholar]
50. Mikuriya Y, Tashiro H, Kobayashi T, Kuroda S, Abe T, Hashimoto Met al. Clinicopathological features of hepatocellular carcinoma in patients with nonalcoholic fatty liver disease. Langenbecks Arch Surg 2015;400:471–476 [DOI] [PubMed] [Google Scholar]
51. Pais R, Fartoux L, Goumard C, Scatton O, Wendum D, Rosmorduc Oet al. Temporal trends, clinical patterns and outcomes of NAFLD-related HCC in patients undergoing liver resection over a 20-year period. Aliment Pharmacol Ther 2017;46:856–863 [DOI] [PubMed] [Google Scholar]
52. Reddy SK, Steel JL, Chen HW, DeMateo DJ, Cardinal J, Behari Jet al. Outcomes of curative treatment for hepatocellular cancer in nonalcoholic steatohepatitis versus hepatitis C and alcoholic liver disease. Hepatology 2012;55:1809–1819 [DOI] [PubMed] [Google Scholar]
53. Su CW, Chau GY, Hung HH, Yeh YC, Lei HJ, Hsia CYet al. Impact of steatosis on prognosis of patients with early-stage hepatocellular carcinoma after hepatic resection. Ann Surg Oncol 2015;22:2253–2261 [DOI] [PubMed] [Google Scholar]
54. Wakai T, Shirai Y, Sakata J, Korita PV, Ajioka Y, Hatakeyama K. Surgical outcomes for hepatocellular carcinoma in nonalcoholic fatty liver disease. J Gastrointest Surg 2011;15:1450–1458 [DOI] [PubMed] [Google Scholar]
55. Wong CR, Njei B, Nguyen MH, Nguyen A, Lim JK. Survival after treatment with curative intent for hepatocellular carcinoma among patients with vs without non-alcoholic fatty liver disease. Aliment Pharmacol Ther 2017;46:1061–1069 [DOI] [PubMed] [Google Scholar]
56. Wu TH, Yu MC, Chan KM, Lee CF, Chen TC, Chang HCet al. Prognostic effect of steatosis on hepatocellular carcinoma patients after liver resection. Eur J Surg Oncol 2011;37:618–622 [DOI] [PubMed] [Google Scholar]
57. Yang T, Hu LY, Li ZL, Liu K, Wu H, Xing Het al. Liver resection for hepatocellular carcinoma in non-alcoholic fatty liver disease: a multicenter propensity matching analysis with HBV-HCC. J Gastrointest Surg 2020;24:320–329 [DOI] [PubMed] [Google Scholar]
58. Yoon JS, Lee HY, Chung SW, Kim SW, Chang Y, Lee YBet al. Prognostic impact of concurrent nonalcoholic fatty liver disease in patients with chronic hepatitis B-related hepatocellular carcinoma. J Gastroenterol Hepatol 2020;35:1960–1968 [DOI] [PubMed] [Google Scholar]
59. D'Silva M, Cho JY, Han HS, Yoon YS, Lee HW, Lee JSet al. Long-term surgical outcomes of non alcoholic fatty liver disease associated hepatocellular carcinoma. Surg Oncol 2022;41:101730 [DOI] [PubMed] [Google Scholar]
60. Xiong KG, Ke KY, Chen LF, Kong JF, Lin TS, Lin QBet al. The impact of metabolic dysfunction-associated fatty liver disease on the prognosis of patients with hepatocellular carcinoma after radical resection. Hepatobiliary Pancreat Dis Int 2022; DOI: 10.1016/j.hbpd.2022.1004.1001[Epub ahead of print] [DOI] [PubMed] [Google Scholar]
61. Zhong JH, Rodriguez AC, Ke Y, Wang YY, Wang L, Li LQ. Hepatic resection as a safe and effective treatment for hepatocellular carcinoma involving a single large tumor, multiple tumors, or macrovascular invasion. Medicine (Baltimore) 2015;94:e396. [DOI] [PMC free article] [PubMed] [Google Scholar]
62. Choo SP, Tan WL, Goh BKP, Tai WM, Zhu AX. Comparison of hepatocellular carcinoma in Eastern versus Western populations. Cancer 2016;122:3430–3446 [DOI] [PubMed] [Google Scholar]
63. Yang JD, Hainaut P, Gores GJ, Amadou A, Plymoth A, Roberts LR. A global view of hepatocellular carcinoma: trends, risk, prevention and management. Nat Rev Gastroenterol Hepatol 2019;16:589–604 [DOI] [PMC free article] [PubMed] [Google Scholar]
64. Zhong JH, Ke Y, Gong WF, Xiang BD, Ma L, Ye XPet al. Hepatic resection associated with good survival for selected patients with intermediate and advanced-stage hepatocellular carcinoma. Ann Surg 2014;260:329–340 [DOI] [PubMed] [Google Scholar]
65. Zhao LY, Huo RR, Xiang X, Torzilli G, Zheng MH, Yang Tet al. Hepatic resection for elderly patients with hepatocellular carcinoma: a systematic review of more than 17,000 patients. Expert Rev Gastroenterol Hepatol 2018;12:1059–1068 [DOI] [PubMed] [Google Scholar]
66. Torzilli G, Belghiti J, Kokudo N, Takayama T, Capussotti L, Nuzzo Get al. A snapshot of the effective indications and results of surgery for hepatocellular carcinoma in tertiary referral centers: is it adherent to the EASL/AASLD recommendations? An observational study of the HCC east-west study group. Ann Surg 2013;257:929–937 [DOI] [PubMed] [Google Scholar]
67. Pfister D, Nunez NG, Pinyol R, Govaere O, Pinter M, Szydlowska Met al. NASH limits anti-tumour surveillance in immunotherapy-treated HCC. Nature 2021;592:450–456 [DOI] [PMC free article] [PubMed] [Google Scholar]
68. Teng YX, Xie S, Guo PP, Deng ZJ, Zhang ZY, Gao Wet al. Hepatocellular carcinoma in non-alcoholic fatty liver disease: current progresses and challenges. J Clin Transl Hepatol 2022;10:955–964 [DOI] [PMC free article] [PubMed] [Google Scholar]
69. Yong JN, Lim WH, Ng CH, Tan DJH, Xiao J, Tay PWLet al. Outcomes of nonalcoholic steatohepatitis after liver transplantation: an updated meta-analysis and systematic review. Clin Gastroenterol Hepatol 2023;21(1):45–54.e6 [DOI] [PubMed] [Google Scholar]
70. Nguyen N, Rode A, Trillaud H, Aube C, Manichon AF, Hocquelet Aet al. Percutaneous radiofrequency ablation for hepatocellular carcinoma developed on non-alcoholic fatty liver disease. Liver Int 2022;42:905–917 [DOI] [PubMed] [Google Scholar]
71. Tan DJH, Ng CH, Lin SY, Pan XH, Tay P, Lim WHet al. Clinical characteristics, surveillance, treatment allocation, and outcomes of non-alcoholic fatty liver disease-related hepatocellular carcinoma: a systematic review and meta-analysis. Lancet Oncol 2022;23:521–530 [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

zrac167_Supplementary_Data

Click here for additional data file.^{(2.5MB, docx)}

Data Availability Statement

All data are in the manuscript. Supplementary material for this article is available online.

References

1. Galle PR, Forner A, Llovet JM, Mazzaferro V, Piscaglia F, Raoul J-Let al. EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 2018;69:182–236 [DOI] [PubMed] [Google Scholar]
2. Zhong JH, Ke Y, Wang YY, Li LQ. Liver resection for patients with hepatocellular carcinoma and macrovascular invasion, multiple tumours, or portal hypertension. Gut 2015;64:520–521 [DOI] [PubMed] [Google Scholar]
3. Yuan BH, Zhu YK, Zou XM, Zhou HD, Li RH, Zhong JH. Repeat hepatic resection versus ablation for patients with recurrent hepatocellular carcinoma: a systematic review. BJS Open 2022;6:zrac036 [DOI] [PMC free article] [PubMed] [Google Scholar]
4. Zhong JH, Xing BC, Zhang WG, Chan AW, Chong CCN, Serenari Met al. Repeat hepatic resection versus radiofrequency ablation for recurrent hepatocellular carcinoma: a retrospective multicentre study. Br J Surg 2022;109:71–78 [DOI] [PubMed] [Google Scholar]
5. Knudsen ES, Gopal P, Singal AG. The changing landscape of hepatocellular carcinoma: etiology, genetics, and therapy. Am J Pathol 2014;184:574–583 [DOI] [PMC free article] [PubMed] [Google Scholar]
6. Wang XY, Huang JM, Lu XM, Harrison TJ, Liu HB, Jia HHet al. Changing risk factors for hepatocellular carcinoma in hyperendemic regions in the era of universal hepatitis B vaccination. Cancer Epidemiol 2020;67:101775 [DOI] [PubMed] [Google Scholar]
7. Tateishi R, Okanoue T, Fujiwara N, Okita K, Kiyosawa K, Omata Met al. Clinical characteristics, treatment, and prognosis of non-B, non-C hepatocellular carcinoma: a large retrospective multicenter cohort study. J Gastroenterol 2015;50:350–360 [DOI] [PMC free article] [PubMed] [Google Scholar]
8. Younossi ZM, Koenig AB, 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 [DOI] [PubMed] [Google Scholar]
9. Eguchi Y, Wong G, Lee IH, Akhtar O, Lopes R, Sumida Y. Hepatocellular carcinoma and other complications of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in Japan: a structured review of published works. Hepatol Res 2021;51:19–30 [DOI] [PubMed] [Google Scholar]
10. Huang DQ, El-Serag HB, Loomba R. Global epidemiology of NAFLD-related HCC: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol 2021;18:223–238 [DOI] [PMC free article] [PubMed] [Google Scholar]
11. Estes C, Anstee QM, Arias-Loste MT, Bantel H, Bellentani S, Caballeria Jet al. Modeling NAFLD disease burden in China, France, Germany, Italy, Japan, Spain, United Kingdom, and United States for the period 2016–2030. J Hepatol 2018;69:896–904 [DOI] [PubMed] [Google Scholar]
12. Orci LA, Sanduzzi-Zamparelli M, Caballol B, Sapena V, Colucci N, Torres Fet al. Incidence of hepatocellular carcinoma in patients with nonalcoholic fatty liver disease: a systematic review, meta-analysis, and meta-regression. Clin Gastroenterol Hepatol 2022;20:283–292.e10 [DOI] [PubMed] [Google Scholar]
13. Le MH, Yeo YH, Li X, Li J, Zou B, Wu Yet al. 2019 Global NAFLD prevalence: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 2022;20:2809–2817.e28 [DOI] [PubMed] [Google Scholar]
14. Teng YX, Liu HT, Deng ZJ, Su JY, Lu YH, Zhong JH. Prevalence of MAFLD-related hepatocellular carcinoma. EJMO 2022;6:190–191 [Google Scholar]
15. Chen J, Song S, Li X, Bian D, Wu X. Association of metabolic traits with occurrence of nonalcoholic fatty liver disease-related hepatocellular carcinoma: a systematic review and meta-analysis of longitudinal cohort studies. Saudi J Gastroenterol 2022;28:92–100 [DOI] [PMC free article] [PubMed] [Google Scholar]
16. Rios RS, Zheng KI, Zheng MH. Non-alcoholic steatohepatitis and risk of hepatocellular carcinoma. Chin Med J (Engl) 2021;134:2911–2921 [DOI] [PMC free article] [PubMed] [Google Scholar]
17. Molinari M, Kaltenmeier C, Samra PB, Liu H, Wessel C, Lou Klem Met al. Hepatic resection for hepatocellular carcinoma in nonalcoholic fatty liver disease: a systematic review and meta-analysis of 7226 patients. Ann Surg Open 2021;2:e065. [DOI] [PMC free article] [PubMed] [Google Scholar]
18. Chin KM, Prieto M, Cheong CK, Di Martino M, Ielpo B, Goh BKPet al. Outcomes after curative therapy for hepatocellular carcinoma in patients with non-alcoholic fatty liver disease: a meta-analysis and review of current literature. HPB (Oxford) 2021;23:1164–1174 [DOI] [PubMed] [Google Scholar]
19. Liu L, Xie S, Teng YX, Deng ZJ, Chen K, Liu HTet al. Outcomes of hepatectomy for metabolic dysfunction-associated fatty liver disease or chronic hepatitis B-related HCC. Front Oncol 2022;11:783339 [DOI] [PMC free article] [PubMed] [Google Scholar]
20. Conci S, Cipriani F, Donadon M, Marchitelli I, Ardito F, Famularo Set al. Hepatectomy for metabolic associated fatty liver disease (MAFLD) related HCC: propensity case-matched analysis with viral- and alcohol-related HCC. Eur J Surg Oncol 2022;48:103–112 [DOI] [PubMed] [Google Scholar]
21. Jung YB, Yoo JE, Han DH, Kim KS, Choi JS, Kim DYet al. Clinical and survival outcomes after hepatectomy in patients with non-alcoholic fatty liver and hepatitis B-related hepatocellular carcinoma. HPB (Oxford) 2021;23:1113–1122 [DOI] [PubMed] [Google Scholar]
22. Lin YP, Lin SH, Wang CC, Lin CC, Chen DW, Chuang CHet al. Impact of MAFLD on HBV-related stage 0/A hepatocellular carcinoma after curative resection. J Pers Med 2021;11:684. [DOI] [PMC free article] [PubMed] [Google Scholar]
23. Cauchy F, Zalinski S, Dokmak S, Fuks D, Farges O, Castera Let al. Surgical treatment of hepatocellular carcinoma associated with the metabolic syndrome. Br J Surg 2013;100:113–121 [DOI] [PubMed] [Google Scholar]
24. Ishizuka M, Kubota K, Kita J, Shimoda M, Kato M, Sawada T. Survival after surgery for hepatocellular carcinoma in relation to presence or absence of viral infection. Am J Surg 2013;206:187–193 [DOI] [PubMed] [Google Scholar]
25. Liang J, Ariizumi SI, Nakano M, Yamamoto M. Diabetes mellitus and/or nonalcoholic steatohepatitis-related hepatocellular carcinoma showed favorable surgical outcomes after hepatectomy. Anticancer Res 2019;39:5639–5643 [DOI] [PubMed] [Google Scholar]
26. Nishio T, Hatano E, Sakurai T, Taura K, Okuno M, Kasai Yet al. Impact of hepatic steatosis on disease-free survival in patients with non-B non-C hepatocellular carcinoma undergoing hepatic resection. Ann Surg Oncol 2015;22:2226–2234 [DOI] [PubMed] [Google Scholar]
27. Tian Y, Lyu H, He Y, Xia Y, Li J, Shen F. Comparison of hepatectomy for patients with metabolic syndrome-related HCC and HBV-related HCC. J Gastrointest Surg 2018;22:615–623 [DOI] [PubMed] [Google Scholar]
28. Vigano L, Conci S, Cescon M, Fava C, Capelli P, D'Errico Aet al. Liver resection for hepatocellular carcinoma in patients with metabolic syndrome: a multicenter matched analysis with HCV-related HCC. J Hepatol 2015;63:93–101 [DOI] [PubMed] [Google Scholar]
29. Lin BZ, Lin TJ, Lin CL, Liao LY, Chang TA, Lu BJet al. Differentiation of clinical patterns and survival outcomes of hepatocellular carcinoma on hepatitis B and nonalcoholic fatty liver disease. J Chin Med Assoc 2021;84:606–613 [DOI] [PubMed] [Google Scholar]
30. Piscaglia F, Svegliati-Baroni G, Barchetti A, Pecorelli A, Marinelli S, Tiribelli Cet al. Clinical patterns of hepatocellular carcinoma in nonalcoholic fatty liver disease: a multicenter prospective study. Hepatology 2016;63:827–838 [DOI] [PubMed] [Google Scholar]
31. Kumar R, Goh BG, Kam JW, Chang PE, Tan CK. Comparisons between non-alcoholic steatohepatitis and alcohol-related hepatocellular carcinoma. Clin Mol Hepatol 2020;26:196–208 [DOI] [PMC free article] [PubMed] [Google Scholar]
32. Weinmann A, Alt Y, Koch S, Nelles C, Duber C, Lang Het al. Treatment and survival of non-alcoholic steatohepatitis associated hepatocellular carcinoma. BMC Cancer 2015;15:210. [DOI] [PMC free article] [PubMed] [Google Scholar]
33. Tokushige K, Hashimoto E, Yatsuji S, Tobari M, Taniai M, Torii Net al. Prospective study of hepatocellular carcinoma in nonalcoholic steatohepatitis in comparison with hepatocellular carcinoma caused by chronic hepatitis C. J Gastroenterol 2010;45:960–967 [DOI] [PubMed] [Google Scholar]
34. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie Det al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA 2000;283:2008–2012 [DOI] [PubMed] [Google Scholar]
35. Eslam M, Newsome PN, Sarin SK, Anstee QM, Targher G, Romero-Gomez Met al. A new definition for metabolic dysfunction-associated fatty liver disease: an international expert consensus statement. J Hepatol 2020;73:202–209 [DOI] [PubMed] [Google Scholar]
36. Eslam M, Sarin SK, Wong VW, Fan JG, Kawaguchi T, Ahn SHet al. The Asian Pacific Association for the Study of the Liver clinical practice guidelines for the diagnosis and management of metabolic associated fatty liver disease. Hepatol Int 2020;14:889–919 [DOI] [PubMed] [Google Scholar]
37. Shiha G, Alswat K, Al Khatry M, Sharara AI, Ormeci N, Waked Iet al. Nomenclature and definition of metabolic-associated fatty liver disease: a consensus from the Middle East and north Africa. Lancet Gastroenterol Hepatol 2021;6:57–64 [DOI] [PubMed] [Google Scholar]
38. Chan WK, Tan SS, Chan SP, Lee YY, Tee HP, Mahadeva Set al. The Malaysian Society of Gastroenterology and hepatology consensus statement on metabolic dysfunction-associated fatty liver disease. J Gastroenterol Hepatol 2022;37:795–811 [DOI] [PMC free article] [PubMed] [Google Scholar]
39. Lim S, Kim JW, Targher G. Links between metabolic syndrome and metabolic dysfunction-associated fatty liver disease. Trends Endocrinol Metab 2021;32:500–514 [DOI] [PubMed] [Google Scholar]
40. Yu C, Wang M, Zheng S, Xia M, Yang H, Zhang Det al. Comparing the diagnostic criteria of MAFLD and NAFLD in the Chinese population: a population-based prospective cohort study. J Clin Transl Hepatol 2022;10:6–16 [DOI] [PMC free article] [PubMed] [Google Scholar]
41. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240:205–213 [DOI] [PMC free article] [PubMed] [Google Scholar]
42. Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos Met al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp (accessed 20 December 2021)
43. Parmar MKB, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med 1998;17:2815–2834 [DOI] [PubMed] [Google Scholar]
44. Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003;327:557–560 [DOI] [PMC free article] [PubMed] [Google Scholar]
45. Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315:629–634 [DOI] [PMC free article] [PubMed] [Google Scholar]
46. Salomao M, Yu WM, Brown RS Jr, Emond JC, Lefkowitch JH. Steatohepatitic hepatocellular carcinoma (SH-HCC): a distinctive histological variant of HCC in hepatitis C virus-related cirrhosis with associated NAFLD/NASH. Am J Surg Pathol 2010;34:1630–1636 [DOI] [PubMed] [Google Scholar]
47. D'Silva M, Na HY, Cho JY, Han HS, Yoon YS, Lee HWet al. Pathological prognostic factors for post-resection survival in patients with hepatocellular carcinoma associated with non-alcoholic fatty liver disease. Transl Cancer Res 2021;10:3345–3355 [DOI] [PMC free article] [PubMed] [Google Scholar]
48. Kimura T, Kobayashi A, Tanaka N, Sano K, Komatsu M, Fujimori Net al. Clinicopathological characteristics of non-B non-C hepatocellular carcinoma without past hepatitis B virus infection. Hepatol Res 2017;47:405–418 [DOI] [PubMed] [Google Scholar]
49. Koh YX, Tan HJ, Liew YX, Syn N, Teo JY, Lee SYet al. Liver resection for nonalcoholic fatty liver disease-associated hepatocellular carcinoma. J Am Coll Surg 2019;229:467–478.e1 [DOI] [PubMed] [Google Scholar]
50. Mikuriya Y, Tashiro H, Kobayashi T, Kuroda S, Abe T, Hashimoto Met al. Clinicopathological features of hepatocellular carcinoma in patients with nonalcoholic fatty liver disease. Langenbecks Arch Surg 2015;400:471–476 [DOI] [PubMed] [Google Scholar]
51. Pais R, Fartoux L, Goumard C, Scatton O, Wendum D, Rosmorduc Oet al. Temporal trends, clinical patterns and outcomes of NAFLD-related HCC in patients undergoing liver resection over a 20-year period. Aliment Pharmacol Ther 2017;46:856–863 [DOI] [PubMed] [Google Scholar]
52. Reddy SK, Steel JL, Chen HW, DeMateo DJ, Cardinal J, Behari Jet al. Outcomes of curative treatment for hepatocellular cancer in nonalcoholic steatohepatitis versus hepatitis C and alcoholic liver disease. Hepatology 2012;55:1809–1819 [DOI] [PubMed] [Google Scholar]
53. Su CW, Chau GY, Hung HH, Yeh YC, Lei HJ, Hsia CYet al. Impact of steatosis on prognosis of patients with early-stage hepatocellular carcinoma after hepatic resection. Ann Surg Oncol 2015;22:2253–2261 [DOI] [PubMed] [Google Scholar]
54. Wakai T, Shirai Y, Sakata J, Korita PV, Ajioka Y, Hatakeyama K. Surgical outcomes for hepatocellular carcinoma in nonalcoholic fatty liver disease. J Gastrointest Surg 2011;15:1450–1458 [DOI] [PubMed] [Google Scholar]
55. Wong CR, Njei B, Nguyen MH, Nguyen A, Lim JK. Survival after treatment with curative intent for hepatocellular carcinoma among patients with vs without non-alcoholic fatty liver disease. Aliment Pharmacol Ther 2017;46:1061–1069 [DOI] [PubMed] [Google Scholar]
56. Wu TH, Yu MC, Chan KM, Lee CF, Chen TC, Chang HCet al. Prognostic effect of steatosis on hepatocellular carcinoma patients after liver resection. Eur J Surg Oncol 2011;37:618–622 [DOI] [PubMed] [Google Scholar]
57. Yang T, Hu LY, Li ZL, Liu K, Wu H, Xing Het al. Liver resection for hepatocellular carcinoma in non-alcoholic fatty liver disease: a multicenter propensity matching analysis with HBV-HCC. J Gastrointest Surg 2020;24:320–329 [DOI] [PubMed] [Google Scholar]
58. Yoon JS, Lee HY, Chung SW, Kim SW, Chang Y, Lee YBet al. Prognostic impact of concurrent nonalcoholic fatty liver disease in patients with chronic hepatitis B-related hepatocellular carcinoma. J Gastroenterol Hepatol 2020;35:1960–1968 [DOI] [PubMed] [Google Scholar]
59. D'Silva M, Cho JY, Han HS, Yoon YS, Lee HW, Lee JSet al. Long-term surgical outcomes of non alcoholic fatty liver disease associated hepatocellular carcinoma. Surg Oncol 2022;41:101730 [DOI] [PubMed] [Google Scholar]
60. Xiong KG, Ke KY, Chen LF, Kong JF, Lin TS, Lin QBet al. The impact of metabolic dysfunction-associated fatty liver disease on the prognosis of patients with hepatocellular carcinoma after radical resection. Hepatobiliary Pancreat Dis Int 2022; DOI: 10.1016/j.hbpd.2022.1004.1001[Epub ahead of print] [DOI] [PubMed] [Google Scholar]
61. Zhong JH, Rodriguez AC, Ke Y, Wang YY, Wang L, Li LQ. Hepatic resection as a safe and effective treatment for hepatocellular carcinoma involving a single large tumor, multiple tumors, or macrovascular invasion. Medicine (Baltimore) 2015;94:e396. [DOI] [PMC free article] [PubMed] [Google Scholar]
62. Choo SP, Tan WL, Goh BKP, Tai WM, Zhu AX. Comparison of hepatocellular carcinoma in Eastern versus Western populations. Cancer 2016;122:3430–3446 [DOI] [PubMed] [Google Scholar]
63. Yang JD, Hainaut P, Gores GJ, Amadou A, Plymoth A, Roberts LR. A global view of hepatocellular carcinoma: trends, risk, prevention and management. Nat Rev Gastroenterol Hepatol 2019;16:589–604 [DOI] [PMC free article] [PubMed] [Google Scholar]
64. Zhong JH, Ke Y, Gong WF, Xiang BD, Ma L, Ye XPet al. Hepatic resection associated with good survival for selected patients with intermediate and advanced-stage hepatocellular carcinoma. Ann Surg 2014;260:329–340 [DOI] [PubMed] [Google Scholar]
65. Zhao LY, Huo RR, Xiang X, Torzilli G, Zheng MH, Yang Tet al. Hepatic resection for elderly patients with hepatocellular carcinoma: a systematic review of more than 17,000 patients. Expert Rev Gastroenterol Hepatol 2018;12:1059–1068 [DOI] [PubMed] [Google Scholar]
66. Torzilli G, Belghiti J, Kokudo N, Takayama T, Capussotti L, Nuzzo Get al. A snapshot of the effective indications and results of surgery for hepatocellular carcinoma in tertiary referral centers: is it adherent to the EASL/AASLD recommendations? An observational study of the HCC east-west study group. Ann Surg 2013;257:929–937 [DOI] [PubMed] [Google Scholar]
67. Pfister D, Nunez NG, Pinyol R, Govaere O, Pinter M, Szydlowska Met al. NASH limits anti-tumour surveillance in immunotherapy-treated HCC. Nature 2021;592:450–456 [DOI] [PMC free article] [PubMed] [Google Scholar]
68. Teng YX, Xie S, Guo PP, Deng ZJ, Zhang ZY, Gao Wet al. Hepatocellular carcinoma in non-alcoholic fatty liver disease: current progresses and challenges. J Clin Transl Hepatol 2022;10:955–964 [DOI] [PMC free article] [PubMed] [Google Scholar]
69. Yong JN, Lim WH, Ng CH, Tan DJH, Xiao J, Tay PWLet al. Outcomes of nonalcoholic steatohepatitis after liver transplantation: an updated meta-analysis and systematic review. Clin Gastroenterol Hepatol 2023;21(1):45–54.e6 [DOI] [PubMed] [Google Scholar]
70. Nguyen N, Rode A, Trillaud H, Aube C, Manichon AF, Hocquelet Aet al. Percutaneous radiofrequency ablation for hepatocellular carcinoma developed on non-alcoholic fatty liver disease. Liver Int 2022;42:905–917 [DOI] [PubMed] [Google Scholar]
71. Tan DJH, Ng CH, Lin SY, Pan XH, Tay P, Lim WHet al. Clinical characteristics, surveillance, treatment allocation, and outcomes of non-alcoholic fatty liver disease-related hepatocellular carcinoma: a systematic review and meta-analysis. Lancet Oncol 2022;23:521–530 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B1] 1. Galle PR, Forner A, Llovet JM, Mazzaferro V, Piscaglia F, Raoul J-Let al. EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 2018;69:182–236 [DOI] [PubMed] [Google Scholar]

[zrac167-B2] 2. Zhong JH, Ke Y, Wang YY, Li LQ. Liver resection for patients with hepatocellular carcinoma and macrovascular invasion, multiple tumours, or portal hypertension. Gut 2015;64:520–521 [DOI] [PubMed] [Google Scholar]

[zrac167-B3] 3. Yuan BH, Zhu YK, Zou XM, Zhou HD, Li RH, Zhong JH. Repeat hepatic resection versus ablation for patients with recurrent hepatocellular carcinoma: a systematic review. BJS Open 2022;6:zrac036 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B4] 4. Zhong JH, Xing BC, Zhang WG, Chan AW, Chong CCN, Serenari Met al. Repeat hepatic resection versus radiofrequency ablation for recurrent hepatocellular carcinoma: a retrospective multicentre study. Br J Surg 2022;109:71–78 [DOI] [PubMed] [Google Scholar]

[zrac167-B5] 5. Knudsen ES, Gopal P, Singal AG. The changing landscape of hepatocellular carcinoma: etiology, genetics, and therapy. Am J Pathol 2014;184:574–583 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B6] 6. Wang XY, Huang JM, Lu XM, Harrison TJ, Liu HB, Jia HHet al. Changing risk factors for hepatocellular carcinoma in hyperendemic regions in the era of universal hepatitis B vaccination. Cancer Epidemiol 2020;67:101775 [DOI] [PubMed] [Google Scholar]

[zrac167-B7] 7. Tateishi R, Okanoue T, Fujiwara N, Okita K, Kiyosawa K, Omata Met al. Clinical characteristics, treatment, and prognosis of non-B, non-C hepatocellular carcinoma: a large retrospective multicenter cohort study. J Gastroenterol 2015;50:350–360 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B8] 8. Younossi ZM, Koenig AB, 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 [DOI] [PubMed] [Google Scholar]

[zrac167-B9] 9. Eguchi Y, Wong G, Lee IH, Akhtar O, Lopes R, Sumida Y. Hepatocellular carcinoma and other complications of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in Japan: a structured review of published works. Hepatol Res 2021;51:19–30 [DOI] [PubMed] [Google Scholar]

[zrac167-B10] 10. Huang DQ, El-Serag HB, Loomba R. Global epidemiology of NAFLD-related HCC: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol 2021;18:223–238 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B11] 11. Estes C, Anstee QM, Arias-Loste MT, Bantel H, Bellentani S, Caballeria Jet al. Modeling NAFLD disease burden in China, France, Germany, Italy, Japan, Spain, United Kingdom, and United States for the period 2016–2030. J Hepatol 2018;69:896–904 [DOI] [PubMed] [Google Scholar]

[zrac167-B12] 12. Orci LA, Sanduzzi-Zamparelli M, Caballol B, Sapena V, Colucci N, Torres Fet al. Incidence of hepatocellular carcinoma in patients with nonalcoholic fatty liver disease: a systematic review, meta-analysis, and meta-regression. Clin Gastroenterol Hepatol 2022;20:283–292.e10 [DOI] [PubMed] [Google Scholar]

[zrac167-B13] 13. Le MH, Yeo YH, Li X, Li J, Zou B, Wu Yet al. 2019 Global NAFLD prevalence: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 2022;20:2809–2817.e28 [DOI] [PubMed] [Google Scholar]

[zrac167-B14] 14. Teng YX, Liu HT, Deng ZJ, Su JY, Lu YH, Zhong JH. Prevalence of MAFLD-related hepatocellular carcinoma. EJMO 2022;6:190–191 [Google Scholar]

[zrac167-B15] 15. Chen J, Song S, Li X, Bian D, Wu X. Association of metabolic traits with occurrence of nonalcoholic fatty liver disease-related hepatocellular carcinoma: a systematic review and meta-analysis of longitudinal cohort studies. Saudi J Gastroenterol 2022;28:92–100 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B16] 16. Rios RS, Zheng KI, Zheng MH. Non-alcoholic steatohepatitis and risk of hepatocellular carcinoma. Chin Med J (Engl) 2021;134:2911–2921 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B17] 17. Molinari M, Kaltenmeier C, Samra PB, Liu H, Wessel C, Lou Klem Met al. Hepatic resection for hepatocellular carcinoma in nonalcoholic fatty liver disease: a systematic review and meta-analysis of 7226 patients. Ann Surg Open 2021;2:e065. [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B18] 18. Chin KM, Prieto M, Cheong CK, Di Martino M, Ielpo B, Goh BKPet al. Outcomes after curative therapy for hepatocellular carcinoma in patients with non-alcoholic fatty liver disease: a meta-analysis and review of current literature. HPB (Oxford) 2021;23:1164–1174 [DOI] [PubMed] [Google Scholar]

[zrac167-B19] 19. Liu L, Xie S, Teng YX, Deng ZJ, Chen K, Liu HTet al. Outcomes of hepatectomy for metabolic dysfunction-associated fatty liver disease or chronic hepatitis B-related HCC. Front Oncol 2022;11:783339 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B20] 20. Conci S, Cipriani F, Donadon M, Marchitelli I, Ardito F, Famularo Set al. Hepatectomy for metabolic associated fatty liver disease (MAFLD) related HCC: propensity case-matched analysis with viral- and alcohol-related HCC. Eur J Surg Oncol 2022;48:103–112 [DOI] [PubMed] [Google Scholar]

[zrac167-B21] 21. Jung YB, Yoo JE, Han DH, Kim KS, Choi JS, Kim DYet al. Clinical and survival outcomes after hepatectomy in patients with non-alcoholic fatty liver and hepatitis B-related hepatocellular carcinoma. HPB (Oxford) 2021;23:1113–1122 [DOI] [PubMed] [Google Scholar]

[zrac167-B22] 22. Lin YP, Lin SH, Wang CC, Lin CC, Chen DW, Chuang CHet al. Impact of MAFLD on HBV-related stage 0/A hepatocellular carcinoma after curative resection. J Pers Med 2021;11:684. [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B23] 23. Cauchy F, Zalinski S, Dokmak S, Fuks D, Farges O, Castera Let al. Surgical treatment of hepatocellular carcinoma associated with the metabolic syndrome. Br J Surg 2013;100:113–121 [DOI] [PubMed] [Google Scholar]

[zrac167-B24] 24. Ishizuka M, Kubota K, Kita J, Shimoda M, Kato M, Sawada T. Survival after surgery for hepatocellular carcinoma in relation to presence or absence of viral infection. Am J Surg 2013;206:187–193 [DOI] [PubMed] [Google Scholar]

[zrac167-B25] 25. Liang J, Ariizumi SI, Nakano M, Yamamoto M. Diabetes mellitus and/or nonalcoholic steatohepatitis-related hepatocellular carcinoma showed favorable surgical outcomes after hepatectomy. Anticancer Res 2019;39:5639–5643 [DOI] [PubMed] [Google Scholar]

[zrac167-B26] 26. Nishio T, Hatano E, Sakurai T, Taura K, Okuno M, Kasai Yet al. Impact of hepatic steatosis on disease-free survival in patients with non-B non-C hepatocellular carcinoma undergoing hepatic resection. Ann Surg Oncol 2015;22:2226–2234 [DOI] [PubMed] [Google Scholar]

[zrac167-B27] 27. Tian Y, Lyu H, He Y, Xia Y, Li J, Shen F. Comparison of hepatectomy for patients with metabolic syndrome-related HCC and HBV-related HCC. J Gastrointest Surg 2018;22:615–623 [DOI] [PubMed] [Google Scholar]

[zrac167-B28] 28. Vigano L, Conci S, Cescon M, Fava C, Capelli P, D'Errico Aet al. Liver resection for hepatocellular carcinoma in patients with metabolic syndrome: a multicenter matched analysis with HCV-related HCC. J Hepatol 2015;63:93–101 [DOI] [PubMed] [Google Scholar]

[zrac167-B29] 29. Lin BZ, Lin TJ, Lin CL, Liao LY, Chang TA, Lu BJet al. Differentiation of clinical patterns and survival outcomes of hepatocellular carcinoma on hepatitis B and nonalcoholic fatty liver disease. J Chin Med Assoc 2021;84:606–613 [DOI] [PubMed] [Google Scholar]

[zrac167-B30] 30. Piscaglia F, Svegliati-Baroni G, Barchetti A, Pecorelli A, Marinelli S, Tiribelli Cet al. Clinical patterns of hepatocellular carcinoma in nonalcoholic fatty liver disease: a multicenter prospective study. Hepatology 2016;63:827–838 [DOI] [PubMed] [Google Scholar]

[zrac167-B31] 31. Kumar R, Goh BG, Kam JW, Chang PE, Tan CK. Comparisons between non-alcoholic steatohepatitis and alcohol-related hepatocellular carcinoma. Clin Mol Hepatol 2020;26:196–208 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B32] 32. Weinmann A, Alt Y, Koch S, Nelles C, Duber C, Lang Het al. Treatment and survival of non-alcoholic steatohepatitis associated hepatocellular carcinoma. BMC Cancer 2015;15:210. [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B33] 33. Tokushige K, Hashimoto E, Yatsuji S, Tobari M, Taniai M, Torii Net al. Prospective study of hepatocellular carcinoma in nonalcoholic steatohepatitis in comparison with hepatocellular carcinoma caused by chronic hepatitis C. J Gastroenterol 2010;45:960–967 [DOI] [PubMed] [Google Scholar]

[zrac167-B34] 34. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie Det al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA 2000;283:2008–2012 [DOI] [PubMed] [Google Scholar]

[zrac167-B35] 35. Eslam M, Newsome PN, Sarin SK, Anstee QM, Targher G, Romero-Gomez Met al. A new definition for metabolic dysfunction-associated fatty liver disease: an international expert consensus statement. J Hepatol 2020;73:202–209 [DOI] [PubMed] [Google Scholar]

[zrac167-B36] 36. Eslam M, Sarin SK, Wong VW, Fan JG, Kawaguchi T, Ahn SHet al. The Asian Pacific Association for the Study of the Liver clinical practice guidelines for the diagnosis and management of metabolic associated fatty liver disease. Hepatol Int 2020;14:889–919 [DOI] [PubMed] [Google Scholar]

[zrac167-B37] 37. Shiha G, Alswat K, Al Khatry M, Sharara AI, Ormeci N, Waked Iet al. Nomenclature and definition of metabolic-associated fatty liver disease: a consensus from the Middle East and north Africa. Lancet Gastroenterol Hepatol 2021;6:57–64 [DOI] [PubMed] [Google Scholar]

[zrac167-B38] 38. Chan WK, Tan SS, Chan SP, Lee YY, Tee HP, Mahadeva Set al. The Malaysian Society of Gastroenterology and hepatology consensus statement on metabolic dysfunction-associated fatty liver disease. J Gastroenterol Hepatol 2022;37:795–811 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B39] 39. Lim S, Kim JW, Targher G. Links between metabolic syndrome and metabolic dysfunction-associated fatty liver disease. Trends Endocrinol Metab 2021;32:500–514 [DOI] [PubMed] [Google Scholar]

[zrac167-B40] 40. Yu C, Wang M, Zheng S, Xia M, Yang H, Zhang Det al. Comparing the diagnostic criteria of MAFLD and NAFLD in the Chinese population: a population-based prospective cohort study. J Clin Transl Hepatol 2022;10:6–16 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B41] 41. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240:205–213 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B42] 42. Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos Met al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp (accessed 20 December 2021)

[zrac167-B43] 43. Parmar MKB, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med 1998;17:2815–2834 [DOI] [PubMed] [Google Scholar]

[zrac167-B44] 44. Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003;327:557–560 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B45] 45. Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315:629–634 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B46] 46. Salomao M, Yu WM, Brown RS Jr, Emond JC, Lefkowitch JH. Steatohepatitic hepatocellular carcinoma (SH-HCC): a distinctive histological variant of HCC in hepatitis C virus-related cirrhosis with associated NAFLD/NASH. Am J Surg Pathol 2010;34:1630–1636 [DOI] [PubMed] [Google Scholar]

[zrac167-B47] 47. D'Silva M, Na HY, Cho JY, Han HS, Yoon YS, Lee HWet al. Pathological prognostic factors for post-resection survival in patients with hepatocellular carcinoma associated with non-alcoholic fatty liver disease. Transl Cancer Res 2021;10:3345–3355 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B48] 48. Kimura T, Kobayashi A, Tanaka N, Sano K, Komatsu M, Fujimori Net al. Clinicopathological characteristics of non-B non-C hepatocellular carcinoma without past hepatitis B virus infection. Hepatol Res 2017;47:405–418 [DOI] [PubMed] [Google Scholar]

[zrac167-B49] 49. Koh YX, Tan HJ, Liew YX, Syn N, Teo JY, Lee SYet al. Liver resection for nonalcoholic fatty liver disease-associated hepatocellular carcinoma. J Am Coll Surg 2019;229:467–478.e1 [DOI] [PubMed] [Google Scholar]

[zrac167-B50] 50. Mikuriya Y, Tashiro H, Kobayashi T, Kuroda S, Abe T, Hashimoto Met al. Clinicopathological features of hepatocellular carcinoma in patients with nonalcoholic fatty liver disease. Langenbecks Arch Surg 2015;400:471–476 [DOI] [PubMed] [Google Scholar]

[zrac167-B51] 51. Pais R, Fartoux L, Goumard C, Scatton O, Wendum D, Rosmorduc Oet al. Temporal trends, clinical patterns and outcomes of NAFLD-related HCC in patients undergoing liver resection over a 20-year period. Aliment Pharmacol Ther 2017;46:856–863 [DOI] [PubMed] [Google Scholar]

[zrac167-B52] 52. Reddy SK, Steel JL, Chen HW, DeMateo DJ, Cardinal J, Behari Jet al. Outcomes of curative treatment for hepatocellular cancer in nonalcoholic steatohepatitis versus hepatitis C and alcoholic liver disease. Hepatology 2012;55:1809–1819 [DOI] [PubMed] [Google Scholar]

[zrac167-B53] 53. Su CW, Chau GY, Hung HH, Yeh YC, Lei HJ, Hsia CYet al. Impact of steatosis on prognosis of patients with early-stage hepatocellular carcinoma after hepatic resection. Ann Surg Oncol 2015;22:2253–2261 [DOI] [PubMed] [Google Scholar]

[zrac167-B54] 54. Wakai T, Shirai Y, Sakata J, Korita PV, Ajioka Y, Hatakeyama K. Surgical outcomes for hepatocellular carcinoma in nonalcoholic fatty liver disease. J Gastrointest Surg 2011;15:1450–1458 [DOI] [PubMed] [Google Scholar]

[zrac167-B55] 55. Wong CR, Njei B, Nguyen MH, Nguyen A, Lim JK. Survival after treatment with curative intent for hepatocellular carcinoma among patients with vs without non-alcoholic fatty liver disease. Aliment Pharmacol Ther 2017;46:1061–1069 [DOI] [PubMed] [Google Scholar]

[zrac167-B56] 56. Wu TH, Yu MC, Chan KM, Lee CF, Chen TC, Chang HCet al. Prognostic effect of steatosis on hepatocellular carcinoma patients after liver resection. Eur J Surg Oncol 2011;37:618–622 [DOI] [PubMed] [Google Scholar]

[zrac167-B57] 57. Yang T, Hu LY, Li ZL, Liu K, Wu H, Xing Het al. Liver resection for hepatocellular carcinoma in non-alcoholic fatty liver disease: a multicenter propensity matching analysis with HBV-HCC. J Gastrointest Surg 2020;24:320–329 [DOI] [PubMed] [Google Scholar]

[zrac167-B58] 58. Yoon JS, Lee HY, Chung SW, Kim SW, Chang Y, Lee YBet al. Prognostic impact of concurrent nonalcoholic fatty liver disease in patients with chronic hepatitis B-related hepatocellular carcinoma. J Gastroenterol Hepatol 2020;35:1960–1968 [DOI] [PubMed] [Google Scholar]

[zrac167-B59] 59. D'Silva M, Cho JY, Han HS, Yoon YS, Lee HW, Lee JSet al. Long-term surgical outcomes of non alcoholic fatty liver disease associated hepatocellular carcinoma. Surg Oncol 2022;41:101730 [DOI] [PubMed] [Google Scholar]

[zrac167-B60] 60. Xiong KG, Ke KY, Chen LF, Kong JF, Lin TS, Lin QBet al. The impact of metabolic dysfunction-associated fatty liver disease on the prognosis of patients with hepatocellular carcinoma after radical resection. Hepatobiliary Pancreat Dis Int 2022; DOI: 10.1016/j.hbpd.2022.1004.1001[Epub ahead of print] [DOI] [PubMed] [Google Scholar]

[zrac167-B61] 61. Zhong JH, Rodriguez AC, Ke Y, Wang YY, Wang L, Li LQ. Hepatic resection as a safe and effective treatment for hepatocellular carcinoma involving a single large tumor, multiple tumors, or macrovascular invasion. Medicine (Baltimore) 2015;94:e396. [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B62] 62. Choo SP, Tan WL, Goh BKP, Tai WM, Zhu AX. Comparison of hepatocellular carcinoma in Eastern versus Western populations. Cancer 2016;122:3430–3446 [DOI] [PubMed] [Google Scholar]

[zrac167-B63] 63. Yang JD, Hainaut P, Gores GJ, Amadou A, Plymoth A, Roberts LR. A global view of hepatocellular carcinoma: trends, risk, prevention and management. Nat Rev Gastroenterol Hepatol 2019;16:589–604 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B64] 64. Zhong JH, Ke Y, Gong WF, Xiang BD, Ma L, Ye XPet al. Hepatic resection associated with good survival for selected patients with intermediate and advanced-stage hepatocellular carcinoma. Ann Surg 2014;260:329–340 [DOI] [PubMed] [Google Scholar]

[zrac167-B65] 65. Zhao LY, Huo RR, Xiang X, Torzilli G, Zheng MH, Yang Tet al. Hepatic resection for elderly patients with hepatocellular carcinoma: a systematic review of more than 17,000 patients. Expert Rev Gastroenterol Hepatol 2018;12:1059–1068 [DOI] [PubMed] [Google Scholar]

[zrac167-B66] 66. Torzilli G, Belghiti J, Kokudo N, Takayama T, Capussotti L, Nuzzo Get al. A snapshot of the effective indications and results of surgery for hepatocellular carcinoma in tertiary referral centers: is it adherent to the EASL/AASLD recommendations? An observational study of the HCC east-west study group. Ann Surg 2013;257:929–937 [DOI] [PubMed] [Google Scholar]

[zrac167-B67] 67. Pfister D, Nunez NG, Pinyol R, Govaere O, Pinter M, Szydlowska Met al. NASH limits anti-tumour surveillance in immunotherapy-treated HCC. Nature 2021;592:450–456 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B68] 68. Teng YX, Xie S, Guo PP, Deng ZJ, Zhang ZY, Gao Wet al. Hepatocellular carcinoma in non-alcoholic fatty liver disease: current progresses and challenges. J Clin Transl Hepatol 2022;10:955–964 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zrac167-B69] 69. Yong JN, Lim WH, Ng CH, Tan DJH, Xiao J, Tay PWLet al. Outcomes of nonalcoholic steatohepatitis after liver transplantation: an updated meta-analysis and systematic review. Clin Gastroenterol Hepatol 2023;21(1):45–54.e6 [DOI] [PubMed] [Google Scholar]

[zrac167-B70] 70. Nguyen N, Rode A, Trillaud H, Aube C, Manichon AF, Hocquelet Aet al. Percutaneous radiofrequency ablation for hepatocellular carcinoma developed on non-alcoholic fatty liver disease. Liver Int 2022;42:905–917 [DOI] [PubMed] [Google Scholar]

[zrac167-B71] 71. Tan DJH, Ng CH, Lin SY, Pan XH, Tay P, Lim WHet al. Clinical characteristics, surveillance, treatment allocation, and outcomes of non-alcoholic fatty liver disease-related hepatocellular carcinoma: a systematic review and meta-analysis. Lancet Oncol 2022;23:521–530 [DOI] [PMC free article] [PubMed] [Google Scholar]

PERMALINK

Prognosis after hepatic resection of patients with hepatocellular carcinoma related to non-alcoholic fatty liver disease: meta-analysis

Jia-Yong Su

Zhu-Jian Deng

Yu-Xian Teng

Ye Xin Koh

Wan-Guang Zhang

Ming-Hua Zheng

Si Xie

Rong-Rui Huo

Chao-Jing Chen

Liang Ma

Jian-Hong Zhong

Abstract

Background

Methods

Results

Conclusion

Introduction

Methods

Inclusion and exclusion criteria

Data sources and literature search strategy

Literature screening and data extraction

Outcomes

Evaluation of study quality

Statistical analysis

Results

Literature search results

Fig. 1.

Characteristics of included studies and patients

Table 1.

Fig. 2.

Perioperative complications and mortality

Overall survival

Fig. 3.

Fig. 4.

Recurrence-free survival

Fig. 5.

Sensitivity analysis

Publication bias

Discussion

Supplementary Material

Acknowledgements

Contributor Information

Funding

Disclosure

Supplementary material

Data availability

References

Associated Data

Supplementary Materials

Data Availability Statement

References

ACTIONS

PERMALINK

RESOURCES

Similar articles

Cited by other articles

Links to NCBI Databases