Clinical and Molecular Hepatology

"Diabetes mellitus"

Original Article

Outcomes of Oral Antidiabetic Drugs in Metabolic Dysfunction-Associated Steatotic Liver Disease: A Nationwide Target Trial Emulation Study: Heejoon Jang, Yeonjin Kim, Yoo Kyoung Lim, Dong Hyeon Lee, Sae Kyung Joo, Bokyung Koo, Woojoo Lee, Stefano Romeo, Won Kim, Innovative Target Exploration of NAFLD (ITEN) consortium; Received September 5, 2025 Accepted December 30, 2025 Published online January 6, 2026; DOI: https://doi.org/10.3350/cmh.2025.1006 [Accepted]

Abstract
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Background/Aims
Patients with concurrent type 2 diabetes mellitus (T2DM) and metabolic dysfunction-associated steatotic liver disease (MASLD) face elevated cardiovascular risks. However, optimal oral antidiabetic drug (OAD) selection for this population remains unclear.
Methods
Using the Korean National Health Information Database, we conducted a target trial emulation comparing cardiovascular outcomes among patients with T2DM and MASLD (defined by fatty liver index ≥30) who initiated sodium-glucose cotransporter 2 (SGLT2) inhibitors, thiazolidinediones, dipeptidyl peptidase-4 (DPP-4) inhibitors, or sulfonylureas with metformin. The primary outcome was major adverse cardiovascular events (MACE), including cardiovascular mortality, nonfatal myocardial infarction, and nonfatal stroke.
Results
Among 71,071 patients (331,726 person-years), SGLT2 inhibitor users experienced a significantly lower MACE risk compared to sulfonylurea users (adjusted subdistribution hazard ratio [aSHR], 0.44; 95% CI, 0.31–0.62). SGLT2 inhibitors also demonstrated a lower MACE risk compared to thiazolidinediones (aSHR, 0.61; 95% CI, 0.39–0.96) and DPP-4 inhibitors (aSHR, 0.59; 95% CI, 0.42–0.96). Cardiovascular mortality risk was notably reduced with SGLT2 inhibitors compared to sulfonylureas (aSHR, 0.13; 95% CI, 0.03-0.50), thiazolidinediones (aSHR, 0.19; 95% CI, 0.04-0.86), and DPP-4 inhibitors (aSHR, 0.22; 95% CI, 0.06-0.84). Mediation analysis revealed that MASLD regression accounted for 8.7% of the total cardiovascular benefit when comparing SGLT2 inhibitors to sulfonylureas.
Conclusions
In patients with concurrent T2DM and MASLD, SGLT2 inhibitors demonstrated better cardiovascular outcomes compared to other OADs. These findings suggest that SGLT2 inhibitors may be the preferred OAD choice for cardiovascular risk reduction in this high-risk population.

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Reply to Correspondence

Advancing metabolic risk profiling in chronic hepatitis B: Reply to correspondence on “Metabolic health in antiviral era of chronic hepatitis B”: Shang-Chin Huang, Jia-Horng Kao; Clin Mol Hepatol 2026;32(1):e117-e118.
Published online May 13, 2025; DOI: https://doi.org/10.3350/cmh.2025.0500

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25 Download

Correspondences

Correspondence to editorial 1 on “Impacts of metabolic syndrome diseases on long-term outcomes of chronic hepatitis B patients treated with nucleos(t)ide analogues”: Rui Huang, Mindie H. Nguyen; Clin Mol Hepatol 2026;32(1):e83-e84.
Published online May 8, 2025; DOI: https://doi.org/10.3350/cmh.2025.0479

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Advancing metabolic risk profiling in chronic hepatitis B: Reply to correspondence on “Metabolic health in antiviral era of chronic hepatitis B”
Shang-Chin Huang, Jia-Horng Kao
Clinical and Molecular Hepatology.2026; 32(1): e117. CrossRef

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Crossref

Correspondence to editorial 2 on “Impacts of metabolic syndrome diseases on long-term outcomes of chronic hepatitis B patients treated with nucleos(t)ide analogues”: Rui Huang, Mindie H. Nguyen; Clin Mol Hepatol 2026;32(1):e85-e86.
Published online May 8, 2025; DOI: https://doi.org/10.3350/cmh.2025.0478

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Editorial

Type 2 diabetes as a key metabolic risk factor for adverse outcomes in nucleos(t)ide analogue-treated chronic hepatitis B: Editorial on “Impacts of metabolic syndrome diseases on long-term outcomes of chronic hepatitis B patients treated with nucleos(t)ide analogues”: Heejoon Jang, Won Kim; Clin Mol Hepatol 2026;32(1):426-428.
Published online April 28, 2025; DOI: https://doi.org/10.3350/cmh.2025.0430

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Correspondence to editorial 2 on “Impacts of metabolic syndrome diseases on long-term outcomes of chronic hepatitis B patients treated with nucleos(t)ide analogues”
Rui Huang, Mindie H. Nguyen
Clinical and Molecular Hepatology.2026; 32(1): e85. CrossRef

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44 Download
Crossref

Correspondence

Viral hepatitis

Correspondence to editorial on “Adverse impact of metabolic dysfunction on fibrosis regression following direct-acting antiviral therapy: A multicenter study for chronic hepatitis C”: Tom Ryu, Young Chang, Seung Up Kim, Jae Young Jang; Clin Mol Hepatol 2025;31(2):e203-e205.
Published online February 24, 2025; DOI: https://doi.org/10.3350/cmh.2025.0179

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Reply to correspondence on “Adverse impact of metabolic dysfunction on fibrosis regression following direct-acting antiviral therapy: A multicenter study for chronic hepatitis C”
Chen-Hua Liu, Yu-Ping Chang
Clinical and Molecular Hepatology.2025; 31(2): e232. CrossRef

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Original Article

Viral hepatitis

Adverse impact of metabolic dysfunction on fibrosis regression following direct-acting antiviral therapy: A multicenter study for chronic hepatitis C: Tom Ryu, Young Chang, Soung Won Jeong, Jeong-Ju Yoo, Sae Hwan Lee, Sang Gyune Kim, Young Seok Kim, Hong Soo Kim, Seung Up Kim, Jae Young Jang; Clin Mol Hepatol 2025;31(2):548-562.
Published online January 9, 2025; DOI: https://doi.org/10.3350/cmh.2024.0904

Background/Aims
Direct-acting antivirals (DAAs) effectively eradicate hepatitis C virus. This study investigated whether metabolic dysfunction influences the likelihood of fibrosis regression after DAA treatment in patients with chronic hepatitis C (CHC).
Methods
This multicenter, retrospective study included 8,819 patients diagnosed with CHC who were treated with DAAs and achieved a sustained virological response (SVR) between January 2014 and December 2022. Fibrosis regression was defined as a 20% reduction in noninvasive surrogates for liver fibrosis, such as liver stiffness (LS) measured by vibration-controlled transient elastography (VCTE) and the fibrosis-4 (FIB-4) score. Hypercholesterolemia (h-TC) was defined as >200 mg/dL.
Results
The median age of the study population was 59.6 years, with a predominance of male patients (n=4,713, 57.3%). Genotypes 1, 2, and others were confirmed in 3,872 (46.2%), 3,487 (41.6%), and 1,024 (12.2%) patients, respectively. Diabetes mellitus (DM) was present in 1,442 (17.2%) patients and the median LS was 7.50 kPa (interquartile range, 5.30–12.50). Multivariate analysis revealed that the presence of DM and pre-DAA h-TC were independently associated with a decreased probability of fibrosis regression by VCTE. Additionally, pre-DAA h-TC was independently associated with a decreased probability of fibrosis regression by the FIB-4.
Conclusions
Metabolic dysfunction has an unfavorable influence on fibrosis regression in patients with CHC who achieve SVR after DAA treatment.

Citations

Citations to this article as recorded by

Editorial: Risk of Incident Type 2 Diabetes and Prediabetes in Patients With Direct Acting Antiviral‐Induced Cure of Hepatitis C Virus Infection—Authors' Reply
Yu‐Ping Chang, Jia‐Horng Kao, Chen‐Hua Liu
Alimentary Pharmacology & Therapeutics.2025; 61(9): 1553. CrossRef
Epidemiologic Characteristics of Chronic Hepatitis B and Coinfections with Hepatitis C Virus or Human Immunodeficiency Virus in South Korea: A Nationwide Claims-Based Study Using the Korean Health Insurance Review and Assessment Service Database
Hyunwoo Oh, Won Sohn, Na Ryung Choi, Hyo Young Lee, Yeonjae Kim, Seung Woo Nam, Jae Yoon Jeong
Pathogens.2025; 14(7): 715. CrossRef

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6 Web of Science
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Correspondence

Steatotic liver disease

Age serves as the silent architect of FIB-4’s precision in unveiling advanced hepatic fibrosis in MASLD with T2DM: Correspondence to letter to the editor on “Diagnostic accuracy of the fibrosis-4 index for advanced liver fibrosis in nonalcoholic fatty liver disease with type 2 diabetes: a systematic review and meta-analysis”: Ji Won Han, Dae Won Jun; Clin Mol Hepatol 2025;31(2):e152-e154.
Published online December 30, 2024; DOI: https://doi.org/10.3350/cmh.2024.1160

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Original Articles

Liver Transplantation

Optimal tacrolimus levels for reducing CKD risk and the impact of intrapatient variability on CKD and ESRD development following liver transplantation: Soon Kyu Lee, Ho Joong Choi, Young Kyoung You, Pil Soo Sung, Seung Kew Yoon, Jeong Won Jang, Jong Young Choi; Clin Mol Hepatol 2025;31(1):131-146.
Published online October 2, 2024; DOI: https://doi.org/10.3350/cmh.2024.0451

Background/Aims
This study aimed to identify the risk factors for chronic kidney disease (CKD) and end-stage renal disease (ESRD) following liver transplantation (LT), with a specific focus on tacrolimus levels and intrapatient variability (IPV).
Methods
Among the 1,076 patients who underwent LT between 2000 and 2018, 952 were included in the analysis. The tacrolimus doses and levels were recorded every 3 months, and the IPV was calculated using the coefficient of variability. The cumulative incidence rates of CKD and ESRD were calculated based on baseline kidney function at the time of LT. The impact of tacrolimus levels and their IPV on the development of CKD and ESRD was evaluated, and the significant risk factors were identified.
Results
Within a median follow-up of 97.3 months, the 5-year cumulative incidence rates of CKD (0.58 vs. 0.24) and ESRD (0.07 vs. 0.01) were significantly higher in the acute kidney injury group than in the normal glomerular filtration rate (GFR) group. In the normal GFR group, the tacrolimus levels were identified as a risk factor for CKD, with a level of ≤4.5 ng/mL suggested as optimal for minimizing the risk of CKD. Furthermore, the IPV of tacrolimus levels and doses emerged as a significant risk factor for CKD development in both groups (p<0.05), with tenofovir disoproxil fumarate also being a risk factor in HBV-infected patients. The IPV of tacrolimus levels was also a significant factor in ESRD development (p<0.05).
Conclusions
This study elucidated the optimal tacrolimus trough level and highlighted the impact of IPV on the CKD and ESRD development post-LT.

Citations

Citations to this article as recorded by

Intrapatient variability of tacrolimus trough level may be not the cause, but an indirect parameter of comorbidities: Editorial on “Optimal tacrolimus levels for reducing CKD risk and the impact of intrapatient variability on CKD and ESRD development foll
Jongman Kim
Clinical and Molecular Hepatology.2025; 31(2): 589. CrossRef
Correspondence to letter to the editor on “Optimal tacrolimus levels for reducing CKD risk and the impact of intrapatient variability on CKD and ESRD development following liver transplantation”
Soon Kyu Lee, Jong Young Choi
Clinical and Molecular Hepatology.2025; 31(2): e212. CrossRef
Clinical significance and gene prediction of a novel classification system based on tacrolimus concentration-to-dose ratio in the early post-liver transplant period
Junwei Fan, Peihao Wen, Liyun Yuan, Yan Xia, Shijie Hu, Xiaoqing Zhang, Zhihai Peng
Frontiers in Pharmacology.2025;[Epub] CrossRef
Chronic kidney disease at one year after liver transplantation: Role of changes in immunosuppression over three decades
Alejandro Muñoz-Serrano, María Jesús Citores, Andrea Gutiérrez-Villanueva, Víctor Moreno-Torres, Jorge V López-Ibor, Natalia Vicente, Valentín Cuervas-Mons
World Journal of Transplantation.2025;[Epub] CrossRef

9,640 View
217 Download
5 Web of Science
Crossref

Viral hepatitis

Prognostic role of computed tomography analysis using deep learning algorithm in patients with chronic hepatitis B viral infection: Jeongin Yoo, Heejin Cho, Dong Ho Lee, Eun Ju Cho, Ijin Joo, Sun Kyung Jeon; Clin Mol Hepatol 2023;29(4):1029-1042.
Published online August 29, 2023; DOI: https://doi.org/10.3350/cmh.2023.0190

Abstract
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Background/Aims
The prediction of clinical outcomes in patients with chronic hepatitis B (CHB) is paramount for effective management. This study aimed to evaluate the prognostic value of computed tomography (CT) analysis using deep learning algorithms in patients with CHB. Methods: This retrospective study included 2,169 patients with CHB without hepatic decompensation who underwent contrast-enhanced abdominal CT for hepatocellular carcinoma (HCC) surveillance between January 2005 and June 2016. Liver and spleen volumes and body composition measurements including subcutaneous adipose tissue (SAT), visceral adipose tissue (VAT), and skeletal muscle indices were acquired from CT images using deep learning-based fully automated organ segmentation algorithms. We assessed the significant predictors of HCC, hepatic decompensation, diabetes mellitus (DM), and overall survival (OS) using Cox proportional hazard analyses. Results: During a median follow-up period of 103.0 months, HCC (n=134, 6.2%), hepatic decompensation (n=103, 4.7%), DM (n=432, 19.9%), and death (n=120, 5.5%) occurred. According to the multivariate analysis, standardized spleen volume significantly predicted HCC development (hazard ratio [HR]=1.01, P=0.025), along with age, sex, albumin and platelet count. Standardized spleen volume (HR=1.01, P<0.001) and VAT index (HR=0.98, P=0.004) were significantly associated with hepatic decompensation along with age and albumin. Furthermore, VAT index (HR=1.01, P=0.001) and standardized spleen volume (HR=1.01, P=0.001) were significant predictors for DM, along with sex, age, and albumin. SAT index (HR=0.99, P=0.004) was significantly associated with OS, along with age, albumin, and MELD. Conclusions: Deep learning-based automatically measured spleen volume, VAT, and SAT indices may provide various prognostic information in patients with CHB.

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Moon Haeng Hur, Jeong-Hoon Lee
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Correspondence to editorial on “Hepatocellular carcinoma prediction model performance decreases with long-term antiviral therapy in chronic hepatitis B patients”
Xiaoqian Xu, Hong You, Jidong Jia, Yuanyuan Kong
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Deep learning assisted biomarker development in patients with chronic hepatitis B: Editorial on “Prognostic role of computed tomography analysis using deep learning algorithm in patients with chronic hepatitis B viral infection”
Yong Eun Chung
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Decreasing performance of HCC prediction models during antiviral therapy for hepatitis B: what else to keep in mind: Editorial on “Hepatocellular carcinoma prediction model performance decreases with long-term antiviral therapy in chronic hepatitis B pati
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Editorial

Steatotic liver disease

Implications of comorbidities in nonalcoholic fatty liver disease: Sherlot Juan Song, Vincent Wai-Sun Wong; Clin Mol Hepatol 2023;29(2):384-389.
Published online March 14, 2023; DOI: https://doi.org/10.3350/cmh.2023.0066

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Meta‐analysis: Efficacy and safety of fibroblast growth factor 21 analogues for the treatment of non‐alcoholic steatohepatitis and non‐alcoholic steatohepatitis‐related fibrosis
Rutao Lin, Jianghua Zhou, Qinmei Sun, Xin Xin, Yiyang Hu, Minghua Zheng, Qin Feng
Alimentary Pharmacology & Therapeutics.2024; 59(7): 802. CrossRef
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Clinical and Molecular Hepatology.2024; 30(3): 561. CrossRef

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2 Web of Science
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Reviews

Steatotic liver disease

Risk factors in nonalcoholic fatty liver disease: Eunji Ko, Eileen L. Yoon, Dae Won Jun; Clin Mol Hepatol 2023;29(Suppl):S79-S85.
Published online December 14, 2022; DOI: https://doi.org/10.3350/cmh.2022.0398

Abstract
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Nonalcoholic fatty liver disease (NAFLD) is the most common liver disease, with a global prevalence estimated at approximately 25%. NAFLD is also the leading cause of liver cirrhosis, hepatocellular carcinoma, and death. Additionally, the risk of cardiovascular disease increases with greater NAFLD severity. The liver- and cardiovascular disease-related mortality incident rate ratios among the NAFLD population were 0.77 and 4.79 per 1,000 person-years, respectively. We intend to discuss the risk factors associated with NAFLD in terms of development and progression. Obesity or higher body mass index is closely associated with NAFLD in a dose-dependent manner, but growing evidence suggests that central obesity plays a more important role in the development of NAFLD. Saturated fat and fructose have been reported to be closely related to NAFLD. Fructose intake promotes lipogenesis and impairs mitochondria fat oxidation. The presence of type 2 diabetes is the most powerful predictive risk factor for hepatic fibrosis in patients with NAFLD. Single nucleotide polymorphism is not only associated with the prevalence of NAFLD but also associated with increased liver disease mortality. Obstructive sleep apnea, intestinal dysbiosis, and sarcopenia are associated with the development of NAFLD

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Steatotic liver disease

Screening strategy for non-alcoholic fatty liver disease: Saisai Zhang, Lung-Yi Mak, Man-Fung Yuen, Wai-Kay Seto; Clin Mol Hepatol 2023;29(Suppl):S103-S122.
Published online November 30, 2022; DOI: https://doi.org/10.3350/cmh.2022.0336

Abstract
PDF

Non-alcoholic fatty liver disease (NAFLD) is the most common chronic liver disease, affecting approximately 25% of the general population worldwide, and is forecasted to increase global health burden in the 21st century. With the advancement of non-invasive tests for assessing and monitoring of steatosis and fibrosis, NAFLD screening is now feasible, and is increasingly highlighted in international guidelines related to hepatology, endocrinology, and pediatrics. Identifying high-risk populations (e.g., diabetes mellitus, obesity, metabolic syndrome) based on risk factors and metabolic characteristics for non-invasive screening is crucial and may aid in designing screening strategies to be more precise and effective. Many screening modalities are currently available, from serum-based methods to ultrasonography, transient elastography, and magnetic resonance imaging, although the diagnostic performance, cost, and accessibility of different methods may impact the actual implementation. A two-step assessment with serum-based fibrosis-4 index followed by imaging test vibration-controlled transient elastography can be an option to stratify the risk of liverrelated complications in NAFLD. There is a need for fibrosis surveillance, as well as investigating the cost-effectiveness of different screening algorithms and engaging primary care for first-stage triage screening.

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Impact of diabetes, obesity, and dyslipidemia on the risk of hepatocellular carcinoma in patients with chronic liver diseases: Hwang Sik Shin, Baek Gyu Jun, Sang-Wook Yi; Clin Mol Hepatol 2022;28(4):773-789.
Published online August 8, 2022; DOI: https://doi.org/10.3350/cmh.2021.0383

Abstract
PDF

Despite the increasing prevalence of metabolic disorders, the potential effects of metabolic factors on hepatocellular carcinoma (HCC) development in individuals with chronic liver diseases (CLDs) are not well understood. For a metabolic factor to be identified as a risk factor for HCC in patients with CLDs, such as hepatitis B virus (HBV) and hepatitis C virus (HCV) infection, there should be a strong synergistic interaction between the carcinogenic mechanisms of the metabolic factor and the CLD itself. This review aims to comprehensively summarize the published data on the relationship between metabolic factors such as diabetes mellitus (DM), obesity, and blood lipids and the risk of HCC in patients with CLDs. DM consistently increases the risk of HCC in patients with CLD. When associated with DM, the risk of HCC seems to be highest in HCV and non-alcoholic fatty liver disease (NAFLD), followed by alcoholic liver disease (ALD) and HBV. Obesity may increase the risk of HCC. Among CLDs, the evidence is relatively consistent and clear for ALD, while clear evidence is limited in other CLDs including HBV, HCV, and NAFLD. Total cholesterol, potentially low-density lipoprotein cholesterol and triglyceride, seems to have strong inverse associations with HCC in individuals with CLDs. Despite evidence from observational studies, statins had no effect in preventing HCC in randomized controlled trials. Whether statins have a preventive effect against HCC is unclear. A better understanding and management of metabolic factors may be beneficial to reduce the risk of HCC in patients with CLDs.

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Hepatic neoplasm

Development and prognosis of hepatocellular carcinoma in patients with diabetes: Takuma Nakatsuka, Ryosuke Tateishi; Clin Mol Hepatol 2023;29(1):51-64.
Published online July 29, 2022; DOI: https://doi.org/10.3350/cmh.2022.0095

Abstract
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The incidence of diabetes mellitus and hepatocellular carcinoma (HCC) has been increasing worldwide during the last few decades, in the context of an increasing prevalence of obesity and non-alcoholic fatty liver disease (NAFLD). Epidemiologic studies have revealed that patients with diabetes have a 2- to 3-fold increased risk of developing HCC, independent of the severity and cause of the underlying liver disease. A bidirectional relationship exists between diabetes and liver disease: advanced liver disease promotes the onset of diabetes, and HCC is an important cause of death in patients with diabetes; conversely, diabetes is a risk factor for liver fibrosis progression and HCC development, and may worsen the long-term prognosis of patients with HCC. The existence of close interconnections among diabetes, obesity, and NAFLD causes insulin resistance-related hyperinsulinemia, increased oxidative stress, and chronic inflammation, which are assumed to be the underlying causes of hepatocarcinogenesis in patients with diabetes. No appropriate surveillance methods for HCC development in patients with diabetes have been established, and liver diseases, including HCC, are often overlooked as complications of diabetes. Although some antidiabetic drugs are expected to prevent HCC development, further research on the optimal use of antidiabetic drugs aimed at hepatoprotection is warranted. Given the increasing medical and socioeconomic impact of diabetes on HCC development, diabetologists and hepatologists need to work together to develop strategies to address this emerging health issue. This article reviews the current knowledge on the impact of diabetes on the development and progression of HCC.

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Original Article

The effect of diabetes and prediabetes on the prevalence, complications and mortality in nonalcoholic fatty liver disease: Cheng Han Ng, Kai En Chan, Yip Han Chin, Rebecca Wenling Zeng, Pei Chen Tsai, Wen Hui Lim, Darren Jun Hao Tan, Chin Meng Khoo, Lay Hoon Goh, Zheng Jye Ling, Anand Kulkarni, Lung-Yi Loey Mak, Daniel Q Huang, Mark Chan, Nicholas WS Chew, Mohammad Shadab Siddiqui, Arun J. Sanyal, Mark Muthiah; Clin Mol Hepatol 2022;28(3):565-574.
Published online May 19, 2022; DOI: https://doi.org/10.3350/cmh.2022.0096

Abstract
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Background/Aims
Nonalcoholic fatty liver disease (NAFLD) is closely associated with diabetes. The cumulative impact of both diseases synergistically increases risk of adverse events. However, present population analysis is predominantly conducted with reference to non-NAFLD individuals and has not yet examined the impact of prediabetes. Hence, we sought to conduct a retrospective analysis on the impact of diabetic status in NAFLD patients, referencing non-diabetic NAFLD individuals.
Methods
Data from the National Health and Nutrition Examination Survey 1999–2018 was used. Hepatic steatosis was defined with United States Fatty Liver Index (US-FLI) and FLI at a cut-off of 30 and 60 respectively, in absence of substantial alcohol use. A multivariate generalized linear model was used for risk ratios of binary outcomes while survival analysis was conducted with Cox regression and Fine Gray model for competing risk.
Results
Of 32,234 patients, 28.92% were identified to have NAFLD. 36.04%, 38.32% and 25.63% were non-diabetic, prediabetic and diabetic respectively. Diabetic NAFLD significantly increased risk of cardiovascular disease (CVD), stroke, chronic kidney disease, all-cause and CVD mortality compared to non-diabetic NAFLD. However, prediabetic NAFLD only significantly increased the risk of CVD and did not result in a higher risk of mortality.
Conclusions
Given the increased risk of adverse outcomes, this study highlights the importance of regular diabetes screening in NAFLD and adoption of prompt lifestyle modifications to reduce disease progression. Facing high cardiovascular burden, prediabetic and diabetic NAFLD individuals can benefit from early cardiovascular referrals to reduce risk of CVD events and mortality.

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Review

Old and new classes of glucose-lowering agents as treatments for non-alcoholic fatty liver disease: A narrative review: Lei Miao, Jing Xu, Giovanni Targher, Christopher D Byrne, Ming-Hua Zheng; Clin Mol Hepatol 2022;28(4):725-738.
Published online March 14, 2022; DOI: https://doi.org/10.3350/cmh.2022.0015

Abstract
PDF

Non-alcoholic fatty liver disease (NAFLD) has become the most common chronic liver disease with a global prevalence of about 55% in people with type 2 diabetes mellitus (T2DM). T2DM, obesity and NAFLD are three closely inter-related pathological conditions. In addition, T2DM is one of the strongest clinical risk factors for the faster progression of NAFLD to non-alcoholic steatohepatitis (NASH), cirrhosis and hepatocellular carcinoma. Increasing evidence suggests that newer classes of glucose-lowering drugs, such as peroxisome proliferator-activated receptor agonists, glucagon-like peptide-1 receptor agonists, dipeptidyl peptidase-4 inhibitors or sodium-glucose cotransporter-2 inhibitors, could reduce the rates of NAFLD progression. This narrative review aims to briefly summarize the recent results from randomized controlled trials testing the efficacy and safety of old and new glucose-lowering drugs for the treatment of NAFLD or NASH in adults both with and without coexisting T2DM.

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Original Article

Steatotic liver disease

Systematic review with meta-analysis: Non-alcoholic fatty liver disease and the association with pregnancy outcomes: Hydar El Jamaly, Guy D Eslick, Martin Weltman; Clin Mol Hepatol 2022;28(1):52-66.
Published online September 17, 2021; DOI: https://doi.org/10.3350/cmh.2021.0205

Background/Aims
Maternal and fetal outcomes in pregnant patients with Non-alcoholic fatty liver disease (NAFLD) have been largely unexplored. To determine the level of evidence associated with maternal and fetal outcomes in pregnant women with NAFLD.
Methods
We conducted a comprehensive literature search. The studies included pregnant patients with a previous, current or subsequent diagnosis of NAFLD. We used a random-effects model using odds ratios (OR) with 95% confidence intervals (CI).
Results
Twenty-two studies, with 13,641 female NAFLD patients were reviewed. The results highlight that NAFLD patients had a statistically significant increased likelihood of baseline diabetes mellitus (OR, 6.00; 95% CI, 2.21–16.31; P<0.001; n=7), baseline Hypertension (OR, 3.75; 95% CI, 2.13–6.59; P<0.001; n=4), gestational hypertension (OR, 1.83; 95% CI, 1.03–3.26; P=0.041; n=2), and pre-eclampsia (OR, 2.43; 95% CI, 1.46–4.04; P=0.001; n=3). The odds for a past and current history of gestational diabetes mellitus were OR, 3.78; 95% CI, 2.21–6.44; P<0.001; n=5 and OR, 3.23; 95% CI, 1.97– 5.31; P<0.001; n=6, respectively. As for fetal outcomes, pregnant NAFLD patients were significantly more likely to have a premature birth (OR, 2.02; 95% CI, 1.44–2.85; P<0.001; n=4), large for gestational age birth (OR, 2.01; 95% CI, 1.72–2.37; P<0.001; n=2) or a history of prior miscarriage or abortion (OR, 1.15; 95% CI, 1.02–1.30; P=0.02; n=2). Egger’s regression revealed no evidence of publication bias (P>0.05).
Conclusions
This meta-analysis provides pooled evidence that NAFLD is associated with a substantial increase in maternal diabetic and hypertensive complications and multiple adverse fetal outcomes. This data is important for clinicians managing these patients before, during and after pregnancy.

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Reviews

Steatotic liver disease

From nonalcoholic fatty liver disease to metabolic-associated fatty liver disease: Big wave or ripple?: Seong Hee Kang, Yuri Cho, Soung Won Jeong, Seung Up Kim, Jin-Woo Lee, On behalf of Korean NAFLD Study Group; Clin Mol Hepatol 2021;27(2):257-269.
Published online March 22, 2021; DOI: https://doi.org/10.3350/cmh.2021.0067

Abstract
PDF

There is some dissatisfaction with the term “nonalcoholic fatty liver disease (NAFLD),” which overemphasizes alcohol and underemphasizes the importance of metabolic risk factors in this disease. Recently, a consensus recommended “metabolic (dysfunction)-associated fatty liver disease (MAFLD)” as a more appropriate term to describe fatty liver diseases (FLD) associated with metabolic dysfunction. During the definition change from NAFLD to MAFLD, subjects with FLD and metabolic abnormalities, together with other etiologies of liver diseases such as alcohol, virus, or medication who have been excluded from the NAFLD criteria, were added to the MAFLD criteria, while subjects with FLD but without metabolic abnormality, who have been included in the NAFLD criteria, were excluded from the MAFLD criteria. This means that there is an emphasis on the metabolic dysfunction in MAFLD which may underestimate the prognostic value of hepatic steatosis itself, whereas the MAFLD criteria might better identify subjects who are at a higher risk of hepatic or cardiovascular outcomes. However, non-metabolic risk NAFLD subjects who are excluded from the MAFLD criteria are missed from the diagnosis, and their potential risk can be the cause of future diseases. Although huge controversies remain, this review focused on summarizing recent studies that compared the clinical and prognostic characteristics between subjects with NAFLD and MAFLD.

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Steatotic liver disease

Beneficial effect of anti-diabetic drugs for nonalcoholic fatty liver disease: Kyung-Soo Kim, Byung-Wan Lee; Clin Mol Hepatol 2020;26(4):430-443.
Published online August 14, 2020; DOI: https://doi.org/10.3350/cmh.2020.0137

Abstract
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Nonalcoholic fatty liver disease (NAFLD) is the most common liver disorder and is associated with various metabolic diseases, including type 2 diabetes mellitus. There are no approved drugs for NAFLD, and the only approved treatment option is weight reduction. As insulin resistance plays an important role in the development of NAFLD, many anti-diabetic drugs have been evaluated for the treatment of NAFLD. Improvement of liver enzymes has been demonstrated by many anti-diabetic drugs, but histological assessment still remains insufficient. Pioglitazone could become the first-line therapy for T2DM patients with NAFLD, based on evidence of histological improvement in patients with biopsy-proven nonalcoholic steatohepatitis (NASH). Liraglutide, another promising alternative, is not yet recommended in patients with NAFLD/NASH due to limited evidence. Therefore, well-designed randomized controlled trials should be performed in the near future to demonstrate if and how anti-diabetic drugs can play a role in the treatment of NAFLD.

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Original Article

Steatotic liver disease

Effects of different exercise modalities on novel hepatic steatosis indices in overweight women with type 2 diabetes: Ebrahim Banitalebi, Mohammad Faramarzi, Samira Nasiri, Majid Mardaniyan, Vahid Rabiee; Clin Mol Hepatol 2019;25(3):294-304.
Published online May 30, 2019; DOI: https://doi.org/10.3350/cmh.2018.0086

Abstract
PDF

Background/Aims
Fatty liver is a clinical and pathologic condition in individuals with type 2 diabetes (T2D). The purpose of this study is to examine the effects of different exercise modalities on non-alcoholic fatty liver indices (fatty liver index [FLI], lipid accumulation product [LAP], hepatic steatosis index [HSI], and Framingham Steatosis Index [FSI]) in women with T2D.
Methods
Fifty-two women with T2D and a mean age of 55.07±5.92 yrs, body mass index (BMI) 28.94±4.09 kg/m2 , and hemoglobin A1c (HbA1c) 9.41±0.82% were randomized to a sprint interval training (SIT) (n=17), combined aerobic and resistance (A+R) training (n=17), or control group (n=18) for 10 weeks. Two-way repeated analysis of variance (ANOVA) was used to find differences between groups and the effects of time and Time×Group interactions after 10 weeks on non-alcoholic fatty liver indices. After this, ANOVA models were constructed to determine the effects of group allocation and change in non-alcoholic fatty liver indices.
Results
There were significant time interactions for FLI (P<0.001), HSI (P<0.001), and LAP (P<0.001). Also, there were significant Time×Group interactions for fasting blood glucose (P=0.034), and HbA1c (P=0.006).
Conclusions
Results highlight that exercise training, independent of mode of training, is an effective strategy to improve some indices related to hepatic steatosis and blood glucose profiles in women with T2D.

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Case Reports

Hepatic involvement of systemic disease

Three cases of glycogenic hepatopathy mimicking acute and relapsing hepatitis in type I diabetes mellitus: Jae Hwang Cha, Sang Ho Ra, Yu Mi Park, Yong Kwan Ji, Ji Hyun Lee, So Yeon Park, Soon Koo Baik, Sang Ok Kwon, Mee Yon Cho, Moon Young Kim; Clin Mol Hepatol 2013;19(4):421-425.
Published online December 28, 2013; DOI: https://doi.org/10.3350/cmh.2013.19.4.421

Abstract
PDF

Glycogenic hepatopathy (GH) is an uncommon cause of serum transaminase elevation in type I diabetes mellitus (DM). The clinical signs and symptoms of GH are nonspecific, and include abdominal discomfort, mild hepatomegaly, and transaminase elevation. In this report we describe three cases of patients presenting serum transaminase elevation and hepatomegaly with a history of poorly controlled type I DM. All of the cases showed sudden elevation of transaminase to more than 30 times the upper normal range (like in acute hepatitis) followed by sustained fluctuation (like in relapsing hepatitis). However, the patients did not show any symptom or sign of acute hepatitis. We therefore performed a liver biopsy to confirm the cause of liver enzyme elevation, which revealed GH. Clinicians should be aware of GH so as to prevent diagnostic delay and misdiagnosis, and have sufficient insight into GH; this will be aided by the present report of three cases along with a literature review.

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Brian K. Cox, Maha Guindi, Danielle Hutchings, Stacey A. Kim, Kevin M. Waters, Brent K. Larson
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Tetiana Glushko, Sergiy V. Kushchayev, Dmitry Trifanov, Aliaksei Salei, Diego Morales, Gerard Berry, Justin Mackey, Oleg M. Teytelboym
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Johad Khoury, Yaniv Zohar, Naim Shehadeh, Tarek Saadi
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Jagannath M Sherigar, Joline De Castro, Yong Mei Yin, Debra Guss, Smruti R Mohanty
World Journal of Hepatology.2018; 10(2): 172. CrossRef
Glycogen Hepatopathy: A Rare and Underrecognized Cause of Recurrent Transaminitis in Patients with Uncontrolled Type 2 Diabetes Mellitus
Kishore Kumar, Shehriyar Mehershahi, Chukwunonso Chime, Hassan Tariq, Suresh Kumar Nayudu, Sridhar Chilimuri
Case Reports in Gastroenterology.2018; 12(2): 466. CrossRef
Four cases of type 1 diabetes mellitus showing sharp serum transaminase increases and hepatomegaly due to glycogenic hepatopathy
Yuichi Ikarashi, Tomomi Kogiso, Etsuko Hashimoto, Kuniko Yamamoto, Kazuhisa Kodama, Makiko Taniai, Nobuyuki Torii, Hiroko Takaike, Yasuko Uchigata, Katsutoshi Tokushige
Hepatology Research.2017;[Epub] CrossRef
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Abhimanyu Chandel, Brittany Scarpato, Jeanette Camacho, Miles McFarland, Shaffer Mok
Case Reports in Hepatology.2017; 2017: 1. CrossRef
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Nishant Parmar, Muslim Atiq, Lee Austin, Ross A. Miller, Thomas Smyrk, Kabir Ahmed
Case Reports in Gastroenterology.2015; 9(2): 221. CrossRef
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Annals of Pediatric Endocrinology & Metabolism.2014; 19(1): 49. CrossRef

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Occurrence of diabetic ketoacidosis and autoimmune thyroiditis in a patient treated with pegylated interferon-alpha 2b and ribavirin for chronic hepatitis C: Yun Nah Lee, M.D., Soung Won Jeong, M.D., Jae Hee Lim, M.D., Yang Seon Ryu, M.D., Seong Ran Jeon, M.D., Sang Kyun Kim, M.D., Jae Young Jang, M.D., Young Seok Kim, M.D., Boo Sung Kim, M.D., Mi Oh Roh, M.D.1; Korean J Hepatol 2010;16(2):187-191.
Published online June 25, 2010; DOI: https://doi.org/10.3350/kjhep.2010.16.2.187

Abstract
PDF

Combined pegylated interferon and ribavirin therapy for chronic hepatitis C infection cause a wide range of side effects, including flu-like syndrome, hematological abnormalities, cardiovascular symptoms, gastrointestinal symptoms, pulmonary dysfunction, depression, and retinopathy. Interferon-alpha has been shown to be related to the development of various autoimmune diseases, including systemic lupus erythematosus, rheumatoid arthritis, autoimmune thyroid disease, and type 1 diabetes mellitus (DM). Type 1 DM and thyroid disease respectively develop in 0.08～2.61% and 10～15% of patients treated with combined interferon-alpha and ribavirin for chronic hepatitis C. The coexistence of type 1 DM and autoimmune thyroiditis was rarely reported. We report a case of a 33-year-old female patient with chronic hepatitis C who simultaneously developed diabetic ketoacidosis and autoimmune thyroiditis after treatment with pegylated interferon-alpha 2b and ribavirin.

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Resolution of Type 2 Diabetes Mellitus Following Interferon-α Therapy for Chronic Hepatitis C
Hee Su Park, Yoon Jung Kim, Soo Yoon Moon, Ji Young Woo, Jae Kyun Choi, Kyung Up Kim, Ju Ri Park, Ho Young Son, Doo-Man Kim
The Journal of Korean Diabetes.2015; 16(4): 315. CrossRef

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Crossref

Original Articles

Clinical features of gas-forming Liver abscesses: comparison between diabetic and nondiabetic patients: Chang Jae Lee, M.D., Sang Young Han, M.D., Sung Wook Lee, M.D., Yang Hyun Baek, M.D., Seok Reyol Choi, M.D., Myung Hwan Roh, M.D., Jong Hoon Lee, M.D., Jin Seok Jang, M.D., Jin Han, M.D., Su Hyun Cho, M.D., Se Woong Choi, M.D.; Korean J Hepatol 2010;16(2):131-138.
Published online June 25, 2010; DOI: https://doi.org/10.3350/kjhep.2010.16.2.131

Abstract
PDF

Background/Aims
Patients with diabetes mellitus (DM) are more likely to have a pyogenic liver abscess with gas formation, which is associated with higher morbidity and mortality. The morbidity and mortality in pyogenic liver abscess are also higher in DM patients than in non-DM patients. This study evaluated the morbidity, mortality, and clinical features in patients with gas-forming liver abscesses associated with DM. Methods: Among 379 cases of pyogenic liver abscess excluding malignancy from January 2001 through December 2009, 25 patients treated for pyogenic-gas-forming liver abscesses were reviewed retrospectively. We compared the morbidity, mortality, and clinical findings in patients with pyogenic-gas-forming liver abscesses between DM and non-DM patients. Results: Gas formation was present in 25 (6.6%) of 379 cases with pyogenic liver abscess. DM was combined with gas-forming liver abscesses in 19 cases (76%). The most common organism responsible for the gas formation was Klebsiella pneumoniae (82%). Complications were present in 23 cases (92%) of gas-forming liver abscesses, with pulmonary complications (especially pleural effusion) being the most common (n=14, 61%). Four patients (16%) died of sepsis. Conclusions: Gas-forming liver abscesses are not uncommon in cases of pyogenic liver abscesses and are associated with high morbidity and mortality rates. The clinical manifestations and complications do not differ significantly between DM and non-DM patients.

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Deepika Sarawat, Gerlin Varghese, Chinmoy Sahu, Nidhi Tejan, Surender Singh, Sangram S. Patel, Mohd R. Khan
Journal of Clinical and Experimental Hepatology.2023; 13(6): 1025. CrossRef
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Bhavish Manwani, Ya Xu, Hana Mohammed El Sahly
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Yong K Kwon, Faiqa A Cheema, Bejon T Maneckshana, Caroline Rochon, Patricia A Sheiner
World Journal of Hepatology.2018; 10(3): 388. CrossRef
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Yuichi Takano, Masafumi Hayashi, Fumitaka Niiya, Toru Nakanishi, Shotaro Hanamura, Kunio Asonuma, Eiichi Yamamura, Kuniyo Gomi, Yuichiro Kuroki, Naotaka Maruoka, Kazuaki Inoue, Masatsugu Nagahama
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Predictors of therapy failure in a series of 741 adult pyogenic liver abscesses
Joseph Zhi Wen Lo, Jeffrey Jia Jun Leow, Perryn Ling Fei Ng, Hui Qi Lee, Nor Alia Mohd Noor, Jee Keem Low, Sameer P. Junnarkar, Winston Wei Liang Woon
Journal of Hepato-Biliary-Pancreatic Sciences.2015; 22(2): 156. CrossRef
Liver abscesses in adult patients with and without diabetes mellitus: an analysis of the clinical characteristics, features of the causative pathogens, outcomes and predictors of fatality: a report based on a large population, retrospective study in China
L.-T. Tian, K. Yao, X.-Y. Zhang, Z.-D. Zhang, Y.-J. Liang, D.-L. Yin, L. Lee, H.-C. Jiang, L.-X. Liu
Clinical Microbiology and Infection.2012; 18(9): E314. CrossRef
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Shih-Chao Kang, Shinn-Jang Hwang
Journal of the Chinese Medical Association.2011; 74(12): 539. CrossRef

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Prevalence and Clinical Significance of Diabetes Mellitus in Patients with Liver Cirrhosis: Kwon So Yeong; Korean J Hepatol 2003;9(3):205-211.

Abstract
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Background/Aims
Impaired glucose tolerance and overt diabetes mellitus (DM) frequently occurs in patients with chronic liver disease. Hyperinsulinaemia and peripheral insulin resistance contribute to the development of DM in these patients. The clinical relevance, however, of DM to their clinical course was not determined. We investigated the prevalence of DM in patients with liver cirrhosis and their chinical characteristics and prognosis. Methods: A total of 606 consecutive cirrhotic patients were enrolled for 5 year. We reviewed all prognosis. findings, clinical courses, and mortality, retrospectively. The cirrhotic patients were divided into two groups according to the presence of DM, and their clinical characteristics and mortality were compared. DM was diagnosed in accordance with National Diabetes Data Group criteria. Results: Among the total of 606 cirrhotic patients (M:F, 482:124), 346 (57.1%) had HBV related disease and 60 (10%) had HCV related disease. Forty-five percent of the patients had a history of habitual drinking. DM was observed in 22.4% of the cirrhotic patients. In the diabetic group, the frequency of HCV infection was significant greater. DM did not affect survival. The DM group, however, appeared to have higher mortality in the patients with Child-Pugh class A cirrhosis during long-term follow up, Only 20.6% of the diabetic patients had normal range blood glucose levels even though most of them received medical therapy, The cases with well controlled blood glucose showed higher survival than poorly controlled cases in the DM group. Conclusions: Cirrhotic patients have a high prevalence of DM, and more frequently are associated with HCV infection. The strict control of blood glucose and the control of infection could be important in prolonging the survival in compensated cirrhotic patients with DM.(Korean J Hepatol 2003;9:205-211)

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Differential Diagnosis of Diabetes Mellitus caused by Liver Cirrhosis and Other Type 2 Diabetes Mellitus: Min Geun Kim , Won Choong Choi; Korean J Hepatol 2006;12(4):524-529.

Abstract
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Background
/Aim: The liver plays important roles in the homeostasis of glucose metabolism since it acts as a major target organ for insulin and a site for gluconeogenesis and glycogen storage. Diabetes mellitus (DM) commonly develops in patients with liver cirrhosis as the result of hepatocyte dysfunction and/or inadequate mass. To assess differences between DM due to liver cirrhosis (hepatogenous DM) and the other type 2 DM, we compared the patterns of hyperglycemia and hyperinsulinemia in hepatogenous DM with those observed in type 2 DM. Methods: 18 diabetic patients with liver cirrhosis (caused by alcohol, n=8; HBV, n=5; HCV, n=2; others, n=3) were matched with 18 type 2 diabetic patients without liver cirrhosis for age and gender. None of the patients or controls had been treated with insulin or β-blockers. The level of glycosylated hemoglobin (HbA1C), fasting plasma glucose (FPG), postprandial plasma glucose (PP2h), fasting plasma C-peptide and insulin were measured. Results: The ratio of PP2h/FPG (2.27 vs. 1.69), fasting insulin (23.2: 11.6 ?IU/mL) and HOMA-IR index (8.38 vs. 3.52) were significantly higher in hepatogenous DM than the other type 2 DM (P<0.05). PP2h, fasting C-peptide and ratio of fasting insulin/C-peptide tend to be higher in hepatogenous DM than those of controls, but which were not statistically significant. Conclusions: The ratio of PP2h/FPG and fasting plasma insulin differentiated hepatogenous DM from the other type 2 DM. Insulin resistance in liver cirrhosis was higher than the other type 2 DM, and impaired hepatic insulin degradation might be an important mechanism of hyperinsulinemia in liver cirrhosis. (Korean J Hepatol 2006;12:524-529)