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Shetty S, Suvarna R, Ambrose Fistus V, Modi S, Pappachan JM. Cardiovascular implications of metabolic dysfunction-associated fatty liver disease and type 2 diabetes mellitus: A meta-analysis. World J Hepatol 2025; 17:105706. [DOI: 10.4254/wjh.v17.i5.105706] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/03/2025] [Revised: 03/31/2025] [Accepted: 04/22/2025] [Indexed: 05/27/2025] Open
Abstract
BACKGROUND Metabolic dysfunction-associated fatty liver disease (MAFLD) and type 2 diabetes mellitus (T2DM) are independent risk factors for the development of cardiovascular disease (CVD) and an exaggerated CVD risk is expected when both diseases co-exist. Therefore, thorough risk stratification is important to inform better clinical practice decisions based on good quality evidence for patient with MAFLD and T2DM.
AIM To identify the CVD and cardiovascular event (CVE) risk in a systematic review when MAFLD and T2DM co-exist to inform better clinical practice decisions.
METHODS A systematic review was performed by compiling data by searching PubMed, EMBASE and Cochrane Library databases. Quality appraisal of retrieved studies and the meta-analysis were performed using Joanna Briggs Institute (JBI) tool and RevMan 5.4 software respectively. The effect indicators for CVE and CVD risk were expressed as odds ratios (OR) and 95%CI with P-values < 0.05 as significant.
RESULTS Fourteen (5 cohort and 9 cross-sectional) studies with 370013 participants were included in this review. The meta-analysis of CVE showed that the risk of CVE in T2DM was higher in the MAFLD group when compared to the non-MAFLD group [OR 1.28 (95%CI, 1.04–1.56) P = 0.02] with follow up duration ranging between 5-6 years. The prevalence of CVD in the metanalysis of cross-sectional studies was found to be higher [OR 1.47 (95%CI, 1.21–1.78) P = 0.0001] in T2DM with MAFLD when compared to T2DM without MAFLD. Significant heterogeneity exists due to variations in study design, methodologies, and MAFLD diagnostic criteria, which may have influenced the study's findings.
CONCLUSION The presence of MAFLD in T2DM increased the risk of CVE. The prevalence of CVD is higher in T2DM with MAFLD as compared to T2DM without MAFLD. Large well-designed multicentric long-term prospective studies are necessary to appropriately risk stratify the cardiovascular effect of the MAFLD in T2DM patients.
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Affiliation(s)
- Sahana Shetty
- Department of Endocrinology, Kasturba Medical College, Manipal, Manipal Academy of Higher Education, Manipal 576104, Karnataka, India
| | - Renuka Suvarna
- Department of Endocrinology, Kasturba Medical College, Manipal, Manipal Academy of Higher Education, Manipal 576104, Karnataka, India
| | - Vanessa Ambrose Fistus
- Department of Medicine, Royal Preston Hospital, Lancashire Teaching Hospitals National Health Service Trust, Preston PR2 9HT, Lancashire, United Kingdom
| | - Shivam Modi
- Department of Endocrinology and Metabolism, Lancashire Teaching Hospitals National Health Service Trust, Preston PR2 9HT, Lancashire, United Kingdom
| | - Joseph M Pappachan
- Faculty of Science, Manchester Metropolitan University, Manchester M15 6BH, United Kingdom
- Department of Endocrinology, Kasturba Medical College, Manipal Academy of Higher Education, Manipal, 576104, India
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Choque Vargas C, Cáceres F, Landeira G, Perez S, Marchi L, Ruffillo G, Tevez S, Puga-Tejada M, Fassio E. Cardiovascular events and incident diabetes in 220 patients with MASLD according to basal liver fibrosis: a 10-year follow-up historic cohort. Eur J Gastroenterol Hepatol 2025; 37:660-667. [PMID: 39975992 DOI: 10.1097/meg.0000000000002943] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/21/2025]
Abstract
AIM The aim of this study is to analyze association between liver fibrosis with CVE, incident diabetes, and cirrhosis complications. METHODS Historic cohort of biopsy-proven MASLD patients, divided into two groups: F0-F2 vs F3-F4 fibrosis. Baseline data included metabolic traits and liver function tests. Patients were contacted and scheduled for laboratory analysis and elastography. Endpoints were (a) CVE, defined as any of acute myocardial infarction, coronary stenting, ischemic cardiopathy, and stroke; (b) incident diabetes; (c) cirrhosis complications. Baseline data were collected at the time of liver biopsy, while follow-up data were recovered through personal interview or medical records. A stepwise logistic regression determined predictive variables for each endpoint. RESULTS Study population included 220 patients with median age 53 years, and 145 were women; baseline fibrosis was F0-F2 in 165 patients and F3-F4 in 55 patients; median follow-up was 9.9 years. A higher percentage of F3-F4 patients had CVE (29.4%) than F0-F2 ones (13.1%) (hazard ratio 2.42; 95% CI: 1.26-4.6; P = 0.008). Incident diabetes occurred in 53.3% of F3-F4 and 20.2% of F0-F2 cohort (hazard ratio 3.04; 95% CI: 1.99-4.86; P < 0.001); cirrhosis complications occurred in 9/55 F3-F4 patients and in 1/165 F0-F2 ones (hazard ratio 26.3; 95% CI: 3.3-208.3; P = 0.002). Multivariate analysis confirmed liver fibrosis as an independent predictor of incident diabetes and cirrhosis complications. CVE were associated with baseline diabetes and aspartate aminotransferase (AST)/alanine aminotransferase (ALT) ratio. CONCLUSION In a cohort of 220 MASLD patients followed for 9.9 years, baseline F3-F4 was associated with incident diabetes and cirrhosis complications. AST/ALT ratio and diabetes were associated with CVE.
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Affiliation(s)
- Cinthia Choque Vargas
- Sección Hígado, Vías Biliares y Páncreas, Servicio de Gastroenterología, Hospital Nacional Prof. Alejandro Posadas, El Palomar, Buenos Aires, Argentina
| | - Francisco Cáceres
- Sección Hígado, Vías Biliares y Páncreas, Servicio de Gastroenterología, Hospital Nacional Prof. Alejandro Posadas, El Palomar, Buenos Aires, Argentina
| | - Graciela Landeira
- Sección Hígado, Vías Biliares y Páncreas, Servicio de Gastroenterología, Hospital Nacional Prof. Alejandro Posadas, El Palomar, Buenos Aires, Argentina
| | - Soledad Perez
- Sección Hígado, Vías Biliares y Páncreas, Servicio de Gastroenterología, Hospital Nacional Prof. Alejandro Posadas, El Palomar, Buenos Aires, Argentina
| | - Laura Marchi
- Sección Hígado, Vías Biliares y Páncreas, Servicio de Gastroenterología, Hospital Nacional Prof. Alejandro Posadas, El Palomar, Buenos Aires, Argentina
| | - Gabriela Ruffillo
- Sección Hígado, Vías Biliares y Páncreas, Servicio de Gastroenterología, Hospital Nacional Prof. Alejandro Posadas, El Palomar, Buenos Aires, Argentina
| | - Silvina Tevez
- Sección Hígado, Vías Biliares y Páncreas, Servicio de Gastroenterología, Hospital Nacional Prof. Alejandro Posadas, El Palomar, Buenos Aires, Argentina
| | - Miguel Puga-Tejada
- Sección Hígado, Vías Biliares y Páncreas, Servicio de Gastroenterología, Hospital Nacional Prof. Alejandro Posadas, El Palomar, Buenos Aires, Argentina
- División de Investigación Médica & Bioestadística, Instituto Ecuatoriano de Enfermedades Digestivas, Guayaquil, Ecuador
| | - Eduardo Fassio
- Sección Hígado, Vías Biliares y Páncreas, Servicio de Gastroenterología, Hospital Nacional Prof. Alejandro Posadas, El Palomar, Buenos Aires, Argentina
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Corica B, Proietti M. Towards a broader perspective on non-alcoholic fatty liver disease and coronary artery disease relationship: managing metabolic risk beyond genetics. Eur J Prev Cardiol 2025:zwaf004. [PMID: 39823217 DOI: 10.1093/eurjpc/zwaf004] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 01/19/2025]
Affiliation(s)
- Bernadette Corica
- Cardiology Division, Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Modena University Hospital, Modena, Italy
- Liverpool Centre for Cardiovascular Science at the University of Liverpool, Liverpool John Moores University, Liverpool Heart & Chest Hospital, Liverpool, UK
| | - Marco Proietti
- Department of Clinical Sciences and Community Health, University of Milan, Via Commenda 19, Milan 20122, Italy
- Division of Subacute Care, IRCCS Istituti Clinici Scientifici Maugeri, Via Camaldoli 64, Milan 20138, Italy
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Jamalinia M, Lonardo A. Perspective article: determinants and assessment of cardiovascular risk in steatotic liver disease owing to metabolic dysfunction-addressing the challenge. METABOLISM AND TARGET ORGAN DAMAGE 2024; 4. [DOI: 10.20517/mtod.2024.34] [Citation(s) in RCA: 2] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/03/2025]
Abstract
Metabolic dysfunction-associated steatotic liver disease (MASLD) stands as an independent risk factor for cardiovascular disease (CVD), which is the leading cause of mortality among MASLD patients. The diverse spectrum of cardio-nephro-metabolic and vascular manifestations inherent in MASLD highlights the complex profile of CVD risk associated with this condition. However, current approaches to assessing CVD risk in MASLD lack specificity, predominantly relying on traditional markers. Although it is widely accepted that patients with advanced fibrosis are more prone to CVD risk, recent evidence suggests that this isolated focus may overlook the remarkable phenotypic variability of this CVD risk across the entire MASLD population. Emerging data indicate a progressive escalation of CVD risk in parallel with the severity of MASLD, highlighting the need for precise disease staging to inform accurate risk assessment. To address this challenge, we propose a novel sequential approach to CVD risk assessment in MASLD. While traditional CVD risk factors remain essential, incorporating liver-specific parameters enhances risk stratification and guides targeted interventions to mitigate the substantial burden of cardiovascular disease in this vulnerable population. This approach involves initial screening using FIB-4 and NAFLD fibrosis score, followed by assessment of liver fibrosis with imaging-based non-invasive techniques in individuals at intermediate-high risk for advanced fibrosis and liver fat quantification in low-risk individuals. Future prospective investigations should focus on the simultaneous use of liver biomarkers and imaging modalities to evaluate, in a sex-specific manner, the efficacy of the proposed approach and to determine optimal thresholds of liver fibrosis and steatosis for optimal CVD risk assessment.
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Liu S, Chen X, Jiang X, Yin X, Fekadu G, Liu C, He Y, Chen H, Ni W, Wang R, Zeng QL, Chen Y, Yang L, Shi R, Ju SH, Shen J, Gao J, Zhao L, Ming WK, Zhong VW, Teng GJ, Qi X. LiverRisk score: An accurate, cost-effective tool to predict fibrosis, liver-related, and diabetes-related mortality in the general population. MED 2024; 5:570-582.e4. [PMID: 38554711 DOI: 10.1016/j.medj.2024.03.003] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/06/2023] [Revised: 01/22/2024] [Accepted: 03/06/2024] [Indexed: 04/02/2024]
Abstract
BACKGROUND Noninvasive and early assessment of liver fibrosis is of great significance and is challenging. We aimed to evaluate the predictive performance and cost-effectiveness of the LiverRisk score for liver fibrosis and liver-related and diabetes-related mortality in the general population. METHODS The general population from the NHANES 2017-March 2020, NHANES 1999-2018, and UK Biobank 2006-2010 were included in the cross-sectional cohort (n = 3,770), along with the NHANES follow-up cohort (n = 25,317) and the UK Biobank follow-up cohort (n = 17,259). The cost-effectiveness analysis was performed using TreeAge Pro software. Liver stiffness measurements ≥10 kPa were defined as compensated advanced chronic liver disease (cACLD). FINDINGS Compared to conventional scores, the LiverRisk score had significantly better accuracy and calibration in predicting liver fibrosis, with an area under the receiver operating characteristic curve (AUC) of 0.76 (0.72-0.79) for cACLD. According to the updated thresholds of LiverRisk score (6 and 10), we reclassified the population into three groups: low, medium, and high risk. The AUCs of LiverRisk score for predicting liver-related and diabetes-related mortality at 5, 10, and 15 years were all above 0.8, with better performance than the Fibrosis-4 score. Furthermore, compared to the low-risk group, the medium-risk and high-risk groups in the two follow-up cohorts had a significantly higher risk of liver-related and diabetes-related mortality. Finally, the cost-effectiveness analysis showed that the incremental cost-effectiveness ratio for LiverRisk score compared to FIB-4 was USD $18,170 per additional quality-adjusted life-year (QALY) gained, below the willingness-to-pay threshold of $50,000/QALY. CONCLUSIONS The LiverRisk score is an accurate, cost-effective tool to predict liver fibrosis and liver-related and diabetes-related mortality in the general population. FUNDING The National Natural Science Foundation of China (nos. 82330060, 92059202, and 92359304); the Key Research and Development Program of Jiangsu Province (BE2023767a); the Fundamental Research Fund of Southeast University (3290002303A2); Changjiang Scholars Talent Cultivation Project of Zhongda Hospital of Southeast University (2023YJXYYRCPY03); and the Research Personnel Cultivation Program of Zhongda Hospital Southeast University (CZXM-GSP-RC125).
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Affiliation(s)
- Shanghao Liu
- Center of Portal Hypertension, Department of Radiology, Zhongda Hospital, Medical School, Southeast University, Nurturing Center of Jiangsu Province for State Laboratory of AI Imaging & Interventional Radiology (Southeast University), Nanjing, China; Basic Medicine Research and Innovation Center of Ministry of Education, Zhongda Hospital, Southeast University, State Key Laboratory of Digital Medical Engineering, Nanjing, China
| | - Xiaohan Chen
- Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Hong Kong SAR, China
| | - Xuanwei Jiang
- Department of Epidemiology and Biostatistics, School of Public Health, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Xiaochun Yin
- Department of Gastroenterology, Zhongda Hospital, Medical School, Southeast University, Nanjing, China
| | - Ginenus Fekadu
- Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Hong Kong SAR, China
| | - Chuan Liu
- Center of Portal Hypertension, Department of Radiology, Zhongda Hospital, Medical School, Southeast University, Nurturing Center of Jiangsu Province for State Laboratory of AI Imaging & Interventional Radiology (Southeast University), Nanjing, China; Basic Medicine Research and Innovation Center of Ministry of Education, Zhongda Hospital, Southeast University, State Key Laboratory of Digital Medical Engineering, Nanjing, China
| | - Yan He
- Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Hong Kong SAR, China
| | - Huihui Chen
- Department of Ultrasound, Zhongda Hospital, Medical School, Southeast University, Nanjing, China
| | - Wenjing Ni
- Department of Infectious Diseases, Nanjing Drum Tower Hospital Clinical College of Nanjing University of Chinese Medicine, Nanjing, China
| | - Ruiying Wang
- The First Clinical Medical College of Lanzhou University, Lanzhou, China
| | - Qing-Lei Zeng
- Department of Infectious Diseases and Hepatology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
| | - Yuping Chen
- Center of Portal Hypertension, Department of Radiology, Zhongda Hospital, Medical School, Southeast University, Nurturing Center of Jiangsu Province for State Laboratory of AI Imaging & Interventional Radiology (Southeast University), Nanjing, China; Basic Medicine Research and Innovation Center of Ministry of Education, Zhongda Hospital, Southeast University, State Key Laboratory of Digital Medical Engineering, Nanjing, China
| | - Ling Yang
- Center of Portal Hypertension, Department of Radiology, Zhongda Hospital, Medical School, Southeast University, Nurturing Center of Jiangsu Province for State Laboratory of AI Imaging & Interventional Radiology (Southeast University), Nanjing, China
| | - Ruihua Shi
- Department of Gastroenterology, Zhongda Hospital, Medical School, Southeast University, Nanjing, China
| | - Sheng-Hong Ju
- Center of Portal Hypertension, Department of Radiology, Zhongda Hospital, Medical School, Southeast University, Nurturing Center of Jiangsu Province for State Laboratory of AI Imaging & Interventional Radiology (Southeast University), Nanjing, China; Basic Medicine Research and Innovation Center of Ministry of Education, Zhongda Hospital, Southeast University, State Key Laboratory of Digital Medical Engineering, Nanjing, China
| | - Jie Shen
- Department of Endocrinology and Metabolism, Shunde Hospital, Southern Medical University (The First People's Hospital of Shunde), Foshan, China
| | - Jingli Gao
- Department of Intensive Care Unit, Kailuan General Hospital, Tangshan, Hebei, China
| | - Linhua Zhao
- Institute of Metabolic Diseases, Guang'anmen Hospital, China Academy of Chinese Medical Sciences, Beijing, China
| | - Wai-Kit Ming
- Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Hong Kong SAR, China
| | - Victor W Zhong
- Department of Epidemiology and Biostatistics, School of Public Health, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Gao-Jun Teng
- Basic Medicine Research and Innovation Center of Ministry of Education, Zhongda Hospital, Southeast University, State Key Laboratory of Digital Medical Engineering, Nanjing, China; Center of Interventional Radiology and Vascular Surgery, Department of Radiology, Zhongda Hospital, Medical School, Southeast University, Nanjing, China.
| | - Xiaolong Qi
- Center of Portal Hypertension, Department of Radiology, Zhongda Hospital, Medical School, Southeast University, Nurturing Center of Jiangsu Province for State Laboratory of AI Imaging & Interventional Radiology (Southeast University), Nanjing, China; Basic Medicine Research and Innovation Center of Ministry of Education, Zhongda Hospital, Southeast University, State Key Laboratory of Digital Medical Engineering, Nanjing, China.
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Zhang SX, Hui DC, Sun MY. Progress in research of type 2 diabetes with nonalcoholic fatty liver in traditional Chinese and Western medicine. Shijie Huaren Xiaohua Zazhi 2024; 32:16-22. [DOI: 10.11569/wcjd.v32.i1.16] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/28/2023] [Revised: 12/24/2023] [Accepted: 01/11/2024] [Indexed: 01/26/2024] Open
Abstract
By analyzing the recent relevant literature on type 2 diabetes with nonalcoholic fatty liver disease, this paper summarizes its etiology, pathogenesis, syndrome differentiation and treatment, clinical treatment, and other aspects from the perspective of traditional Chinese medicine (TCM) and Western medicine. There has been some progress in the treatment of this disease in both TCM and Western medicine, but further in-depth study is required to explore its pathogenesis. Moreover, the etiology, pathogenesis, and syndrome differentiation of this disease in TCM are not yet unified, and large-scale, multicenter, and prospective clinical research is insufficient. There is also a lack of research on the action and targets of TCM in this disease.
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Affiliation(s)
- Shun-Xiao Zhang
- Department of Endocrinology, Shanghai Baoshan District Hospital of Integrated Traditional Chinese and Western Medicine, Shanghai 201999, China
| | - Deng-Cheng Hui
- Key Laboratory of Liver and Kidney Diseases, Ministry of Education, Institute of Liver Diseases, Shanghai University of Traditional Chinese Medicine, Shanghai 201203, China
- Department of Liver Diseases, Shuguang Hospital Affiliated to Shanghai University of Traditional Chinese Medicine, Shanghai 201203, China
| | - Ming-Yu Sun
- Key Laboratory of Liver and Kidney Diseases, Ministry of Education, Institute of Liver Diseases, Shanghai University of Traditional Chinese Medicine, Shanghai 201203, China
- Department of Liver Diseases, Shuguang Hospital Affiliated to Shanghai University of Traditional Chinese Medicine, Shanghai 201203, China
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Suwała S, Białczyk A, Koperska K, Rajewska A, Krintus M, Junik R. Prevalence and Crucial Parameters in Diabesity-Related Liver Fibrosis: A Preliminary Study. J Clin Med 2023; 12:7760. [PMID: 38137829 PMCID: PMC10744287 DOI: 10.3390/jcm12247760] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/03/2023] [Revised: 11/28/2023] [Accepted: 12/16/2023] [Indexed: 12/24/2023] Open
Abstract
Diabetes and obesity have been recognized as confirmed risk factors for the occurrence of liver fibrosis. Despite the long-standing acknowledgment of "diabesity", the simultaneous existence of diabetes and obesity, scholarly literature has shown limited attention to this topic. The aim of this pilot study was to assess the prevalence of liver fibrosis among individuals with diabetes (specifically those who are obese) in order to identify the key factors associated with hepatofibrosis and determine the most important associations and differences between patients with and without liver fibrosis. The research included a total of 164 participants (48.17% had comorbid obesity). Liver elastography (Fibroscan) was performed on these individuals in addition to laboratory tests. Liver fibrosis was found in 34.76% of type 2 diabetes patients; male gender almost doubled the risk of hepatofibrosis (RR 1.81) and diabesity nearly tripled this risk (RR 2.81; however, in degree III of obesity, the risk was elevated to 3.65 times higher). Anisocytosis, thrombocytopenia, or elevated liver enzymes raised the incidence of liver fibrosis by 1.78 to 2.47 times. In these individuals, liver stiffness was negatively correlated with MCV, platelet count, and albumin concentration; GGTP activity and HbA1c percentage were positively correlated. The regression analysis results suggest that the concentration of albumin and the activity of GGTP are likely to have a substantial influence on the future management of liver fibrosis in patients with diabesity. The findings of this study can serve as the basis for subsequent investigations and actions focused on identifying potential therapeutic and diagnostic avenues.
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Affiliation(s)
- Szymon Suwała
- Department of Endocrinology and Diabetology, Nicolaus Copernicus University, Collegium Medicum, 9 Sklodowskiej-Curie Street, 85-094 Bydgoszcz, Poland;
| | - Aleksandra Białczyk
- Evidence-Based Medicine Students Scientific Club of Department of Endocrinology and Diabetology, Nicolaus Copernicus University, Collegium Medicum, 9 Sklodowskiej-Curie Street, 85-094 Bydgoszcz, Poland; (A.B.); (K.K.); (A.R.)
| | - Kinga Koperska
- Evidence-Based Medicine Students Scientific Club of Department of Endocrinology and Diabetology, Nicolaus Copernicus University, Collegium Medicum, 9 Sklodowskiej-Curie Street, 85-094 Bydgoszcz, Poland; (A.B.); (K.K.); (A.R.)
| | - Alicja Rajewska
- Evidence-Based Medicine Students Scientific Club of Department of Endocrinology and Diabetology, Nicolaus Copernicus University, Collegium Medicum, 9 Sklodowskiej-Curie Street, 85-094 Bydgoszcz, Poland; (A.B.); (K.K.); (A.R.)
| | - Magdalena Krintus
- Department of Laboratory Medicine, Nicolaus Copernicus University, Collegium Medicum, 9 Sklodowskiej-Curie Street, 85-094 Bydgoszcz, Poland;
| | - Roman Junik
- Department of Endocrinology and Diabetology, Nicolaus Copernicus University, Collegium Medicum, 9 Sklodowskiej-Curie Street, 85-094 Bydgoszcz, Poland;
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Kim BK, Bergstrom J, Loomba R, Tamaki N, Izumi N, Nakajima A, Idilman R, Gumussoy M, Oz DK, Erden A, Truong E, Yang JD, Noureddin M, Allen AM, Loomba R, Ajmera V. Magnetic resonance elastography-based prediction model for hepatic decompensation in NAFLD: A multicenter cohort study. Hepatology 2023; 78:1858-1866. [PMID: 37203233 PMCID: PMC10663382 DOI: 10.1097/hep.0000000000000470] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/20/2023] [Accepted: 04/29/2023] [Indexed: 05/20/2023]
Abstract
BACKGROUND AND AIMS Magnetic resonance elastography (MRE) is an accurate, continuous biomarker of liver fibrosis; however, the optimal combination with clinical factors to predict the risk of incident hepatic decompensation is unknown. Therefore, we aimed to develop and validate an MRE-based prediction model for hepatic decompensation for patients with NAFLD. APPROACH AND RESULTS This international multicenter cohort study included participants with NAFLD undergoing MRE from 6 hospitals. A total of 1254 participants were randomly assigned as training (n = 627) and validation (n = 627) cohorts. The primary end point was hepatic decompensation, defined as the first occurrence of variceal hemorrhage, ascites, or HE. Covariates associated with hepatic decompensation on Cox-regression were combined with MRE to construct a risk prediction model in the training cohort and then tested in the validation cohort. The median (IQR) age and MRE values were 61 (18) years and 3.5 (2.5) kPa in the training cohort and 60 (20) years and 3.4 (2.5) kPa in the validation cohort, respectively. The MRE-based multivariable model that included age, MRE, albumin, aspartate aminotransferase, and platelets had excellent discrimination for the 3- and 5-year risk of hepatic decompensation (c-statistic 0.912 and 0.891, respectively) in the training cohort. The diagnostic accuracy remained consistent in the validation cohort with a c-statistic of 0.871 and 0.876 for hepatic decompensation at 3 and 5 years, respectively, and was superior to Fibrosis-4 in both cohorts ( p < 0.05). CONCLUSIONS An MRE-based prediction model allows for accurate prediction of hepatic decompensation and assists in the risk stratification of patients with NAFLD.
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Affiliation(s)
- Beom Kyung Kim
- NAFLD Research Center, Division of Gastroenterology. University of California at San Diego, La Jolla, CA, USA
- Department of Internal Medicine, Yonsei University College of Medicine, Seoul, Republic of Korea
| | - Jaclyn Bergstrom
- NAFLD Research Center, Division of Gastroenterology. University of California at San Diego, La Jolla, CA, USA
| | - Rohan Loomba
- NAFLD Research Center, Division of Gastroenterology. University of California at San Diego, La Jolla, CA, USA
| | - Nobuharu Tamaki
- NAFLD Research Center, Division of Gastroenterology. University of California at San Diego, La Jolla, CA, USA
- Department of Gastroenterology and Hepatology, Musashino Red Cross Hospital Tokyo, Japan
| | - Namiki Izumi
- Department of Gastroenterology and Hepatology, Musashino Red Cross Hospital Tokyo, Japan
| | - Atsushi Nakajima
- Department of Gastroenterology and Hepatology, Yokohama City University, Yokohama, Japan
| | - Ramazan Idilman
- Ankara University School of Medicine, Department of Gastroenterology, Ankara Turkey
| | - Mesut Gumussoy
- Ankara University School of Medicine, Department of Gastroenterology, Ankara Turkey
| | - Digdem Kuru Oz
- Ankara University School of Medicine, Department of Radiology, Ankara Turkey
| | - Ayse Erden
- Ankara University School of Medicine, Department of Radiology, Ankara Turkey
| | - Emily Truong
- Department of Gastroenterology and Hepatology, Cedars Sinai, Los Angeles, CA, USA
| | - Ju Dong Yang
- Department of Gastroenterology and Hepatology, Cedars Sinai, Los Angeles, CA, USA
| | - Mazen Noureddin
- Department of Gastroenterology and Hepatology, Cedars Sinai, Los Angeles, CA, USA
| | - Alina M. Allen
- Division of Gastroenterology and Hepatology, Mayo Clinic, Rochester, MN, USA
| | - Rohit Loomba
- NAFLD Research Center, Division of Gastroenterology. University of California at San Diego, La Jolla, CA, USA
- School of Public Health, University of California, San Diego
| | - Veeral Ajmera
- NAFLD Research Center, Division of Gastroenterology. University of California at San Diego, La Jolla, CA, USA
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Roca-Fernandez A, Banerjee R, Thomaides-Brears H, Telford A, Sanyal A, Neubauer S, Nichols TE, Raman B, McCracken C, Petersen SE, Ntusi NA, Cuthbertson DJ, Lai M, Dennis A, Banerjee A. Liver disease is a significant risk factor for cardiovascular outcomes - A UK Biobank study. J Hepatol 2023; 79:1085-1095. [PMID: 37348789 DOI: 10.1016/j.jhep.2023.05.046] [Citation(s) in RCA: 55] [Impact Index Per Article: 27.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/21/2022] [Revised: 05/25/2023] [Accepted: 05/31/2023] [Indexed: 06/24/2023]
Abstract
BACKGROUND & AIMS Chronic liver disease (CLD) is associated with increased cardiovascular disease (CVD) risk. We investigated whether early signs of liver disease (measured by iron-corrected T1-mapping [cT1]) were associated with an increased risk of major CVD events. METHODS Liver disease activity (cT1) and fat (proton density fat fraction [PDFF]) were measured using LiverMultiScan® between January 2016 and February 2020 in the UK Biobank imaging sub-study. Using multivariable Cox regression, we explored associations between liver cT1 (MRI) and primary CVD (coronary artery disease, atrial fibrillation [AF], embolism/vascular events, heart failure [HF] and stroke), and CVD hospitalisation and all-cause mortality. Liver blood biomarkers, general metabolism biomarkers, and demographics were also included. Subgroup analysis was conducted in those without metabolic syndrome (defined as at least three of: a large waist, high triglycerides, low high-density lipoprotein cholesterol, increased systolic blood pressure, or elevated haemoglobin A1c). RESULTS A total of 33,616 participants (mean age 65 years, mean BMI 26 kg/m2, mean haemoglobin A1c 35 mmol/mol) had complete MRI liver data with linked clinical outcomes (median time to major CVD event onset: 1.4 years [range: 0.002-5.1]; follow-up: 2.5 years [range: 1.1-5.2]). Liver disease activity (cT1), but not liver fat (PDFF), was associated with higher risk of any major CVD event (hazard ratio 1.14; 95% CI 1.03-1.26; p = 0.008), AF (1.30; 1.12-1.51; p <0.001); HF (1.30; 1.09-1.56; p= 0.004); CVD hospitalisation (1.27; 1.18-1.37; p <0.001) and all-cause mortality (1.19; 1.02-1.38; p = 0.026). FIB-4 index was associated with HF (1.06; 1.01-1.10; p = 0.007). Risk of CVD hospitalisation was independently associated with cT1 in individuals without metabolic syndrome (1.26; 1.13-1.4; p <0.001). CONCLUSION Liver disease activity, by cT1, was independently associated with a higher risk of incident CVD and all-cause mortality, independent of pre-existing metabolic syndrome, liver fibrosis or fat. IMPACT AND IMPLICATIONS Chronic liver disease (CLD) is associated with a twofold greater incidence of cardiovascular disease. Our work shows that early liver disease on iron-corrected T1 mapping was associated with a higher risk of major cardiovascular disease (14%), cardiovascular disease hospitalisation (27%) and all-cause mortality (19%). These findings highlight the prognostic relevance of a comprehensive evaluation of liver health in populations at risk of CVD and/or CLD, even in the absence of clinical manifestations or metabolic syndrome, when there is an opportunity to modify/address risk factors and prevent disease progression. As such, they are relevant to patients, carers, clinicians, and policymakers.
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Affiliation(s)
| | - Rajarshi Banerjee
- Perspectum Ltd., Oxford, United Kingdom; Oxford University Hospitals Foundation Trust, Oxford, United Kingdom
| | | | | | - Arun Sanyal
- Division of Gastroenterology, Hepatology and Nutrition, Virginia Commonwealth University School of Medicine, Richmond, VA, United States
| | - Stefan Neubauer
- Division of Cardiovascular Medicine, Radcliffe Department of Medicine, University of Oxford, United Kingdom
| | - Thomas E Nichols
- Big Data Institute, Li Ka Shing Centre for Health Information and Discovery, Nuffield Department of Population Health, University of Oxford, Oxford, UK
| | - Betty Raman
- Oxford University Hospitals Foundation Trust, Oxford, United Kingdom; Division of Cardiovascular Medicine, Radcliffe Department of Medicine, University of Oxford, United Kingdom
| | - Celeste McCracken
- Division of Cardiovascular Medicine, Radcliffe Department of Medicine, University of Oxford, United Kingdom
| | - Steffen E Petersen
- William Harvey Research Institute, NIHR Barts Biomedical Research Centre, Queen Mary University London, Charterhouse Square, London, United Kingdom; Barts Heart Centre, St Bartholomew's Hospital, Barts Health NHS Trust, West Smithfield, London, UK; Health Data Research UK, London, UK; Alan Turing Institute, London, UK
| | - Ntobeko Ab Ntusi
- Division of Cardiology, Department of Medicine, University of Cape Town and Groote Schuur, J46, Old Main Building, Main Road, Observatory, Cape Town, 7925, South Africa
| | - Daniel J Cuthbertson
- Department of Cardiovascular and Metabolic Medicine, Institute of Life Course and Medical Sciences, University of Liverpool, Liverpool, UK; Liverpool University Hospitals NHS Foundation Trust, Liverpool, UK
| | - Michele Lai
- Department of Medicine, Liver Centre, Beth Israel Deaconess Medical Centre, Harvard Medical School, 110 Francis Street, Suite 4A, Boston, USA
| | | | - Amitava Banerjee
- University College London Hospitals National Health Service Trust, London, United Kingdom; Institute of Health Informatics, University College London, London, United Kingdom; Barts Health National Health Service Trust, The Royal London Hospital, London, United Kingdom.
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10
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En Li Cho E, Ang CZ, Quek J, Fu CE, Lim LKE, Heng ZEQ, Tan DJH, Lim WH, Yong JN, Zeng R, Chee D, Nah B, Lesmana CRA, Bwa AH, Win KM, Faulkner C, Aboona MB, Lim MC, Syn N, Kulkarni AV, Suzuki H, Takahashi H, Tamaki N, Wijarnpreecha K, Huang DQ, Muthiah M, Ng CH, Loomba R. Global prevalence of non-alcoholic fatty liver disease in type 2 diabetes mellitus: an updated systematic review and meta-analysis. Gut 2023; 72:2138-2148. [PMID: 37491159 DOI: 10.1136/gutjnl-2023-330110] [Citation(s) in RCA: 101] [Impact Index Per Article: 50.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/18/2023] [Accepted: 06/20/2023] [Indexed: 07/27/2023]
Abstract
INTRODUCTION Non-alcoholic fatty liver disease (NAFLD) is the leading cause of chronic liver disease, with type 2 diabetes mellitus (T2DM) as a major predictor. Insulin resistance and chronic inflammation are key pathways in the pathogenesis of T2DM leading to NAFLD and vice versa, with the synergistic effect of NAFLD and T2DM increasing morbidity and mortality risks. This meta-analysis aims to quantify the prevalence of NAFLD and the prevalence of clinically significant and advanced fibrosis in people with T2DM. METHODS MEDLINE and Embase databases were searched from inception until 13 February 2023. The primary outcomes were the prevalence of NAFLD, non-alcoholic steatohepatitis (NASH) and fibrosis in people with T2DM. A generalised linear mixed model with Clopper-Pearson intervals was used for the analysis of proportions with sensitivity analysis conducted to explore heterogeneity between studies. RESULTS 156 studies met the inclusion criteria, and a pooled analysis of 1 832 125 patients determined that the prevalence rates of NAFLD and NASH in T2DM were 65.04% (95% CI 61.79% to 68.15%, I2=99.90%) and 31.55% (95% CI 17.12% to 50.70%, I2=97.70%), respectively. 35.54% (95% CI 19.56% to 55.56%, I2=100.00%) of individuals with T2DM with NAFLD had clinically significant fibrosis (F2-F4), while 14.95% (95% CI 11.03% to 19.95%, I2=99.00%) had advanced fibrosis (F3-F4). CONCLUSION This study determined a high prevalence of NAFLD, NASH and fibrosis in people with T2DM. Increased efforts are required to prevent T2DM to combat the rising burden of NAFLD. PROSPERO REGISTRATION NUMBER CRD42022360251.
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Affiliation(s)
- Elina En Li Cho
- Department of Medicine, National University Hospital, Singapore
| | - Chong Zhe Ang
- Department of Medicine, National University Hospital, Singapore
| | - Jingxuan Quek
- Yong Loo Lin School of Medicine, National University of Singapore, Singapore
| | - Clarissa Elysia Fu
- Yong Loo Lin School of Medicine, National University of Singapore, Singapore
| | - Lincoln Kai En Lim
- Yong Loo Lin School of Medicine, National University of Singapore, Singapore
| | - Zane En Qi Heng
- Yong Loo Lin School of Medicine, National University of Singapore, Singapore
| | - Darren Jun Hao Tan
- Yong Loo Lin School of Medicine, National University of Singapore, Singapore
| | - Wen Hui Lim
- Yong Loo Lin School of Medicine, National University of Singapore, Singapore
| | - Jie Ning Yong
- Yong Loo Lin School of Medicine, National University of Singapore, Singapore
| | - Rebecca Zeng
- Yong Loo Lin School of Medicine, National University of Singapore, Singapore
| | - Douglas Chee
- Department of Medicine, National University Hospital, Singapore
| | - Benjamin Nah
- Department of Medicine, National University Hospital, Singapore
| | | | - Aung Hlaing Bwa
- Department of Medical Research, Union of Myanmar, Naypyidaw, Myanmar
| | - Khin Maung Win
- Department of Medical Research, Union of Myanmar, Naypyidaw, Myanmar
| | - Claire Faulkner
- Department of Medicine, University of Arizona College of Medicine, Phoenix, Arizona, USA
| | - Majd B Aboona
- Department of Medicine, University of Arizona College of Medicine, Phoenix, Arizona, USA
| | - Mei Chin Lim
- Yong Loo Lin School of Medicine, National University of Singapore, Singapore
- Department of Diagnostic Imaging, National University Health System, Singapore
| | - Nicholas Syn
- Yong Loo Lin School of Medicine, National University of Singapore, Singapore
| | - Anand V Kulkarni
- Hepatology, Asian Institute of Gastroenterology, Hyderabad, Telangana, India
| | - Hiroyuki Suzuki
- Department of Medicine, Kurume University School of Medicine, Kurume, Japan
| | | | - Nobuharu Tamaki
- Department of Medicine, University of California San Diego, La Jolla, California, USA
- Department of Medicine, Musashino Red Cross Hospital, Musashino, Japan
| | - Karn Wijarnpreecha
- Division of Gastroenterology and Hepatology, University of Michigan, Michigan, Michigan, USA
| | - Daniel Q Huang
- Department of Medicine, National University Hospital, Singapore
- Yong Loo Lin School of Medicine, National University of Singapore, Singapore
- Division of Gastroenterology and Hepatology, National University Health System, Singapore
| | - Mark Muthiah
- Department of Medicine, National University Hospital, Singapore
- Yong Loo Lin School of Medicine, National University of Singapore, Singapore
- Division of Gastroenterology and Hepatology, National University Health System, Singapore
| | - Cheng Han Ng
- Yong Loo Lin School of Medicine, National University of Singapore, Singapore
| | - Rohit Loomba
- Department of Medicine, University of California San Diego, La Jolla, California, USA
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11
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Lu C, Chen Y, Zhang Y, Zhao X. Liver Fibrosis Scores and Coronary Artery Disease: Novel Findings in Patients with Metabolic Dysfunction-Associated Fatty Liver Disease. Diabetes Metab Syndr Obes 2023; 16:2627-2637. [PMID: 37663203 PMCID: PMC10474841 DOI: 10.2147/dmso.s426102] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/15/2023] [Accepted: 08/21/2023] [Indexed: 09/05/2023] Open
Abstract
Background Metabolic dysfunction-associated fatty liver disease (MAFLD) is a recently proposed term as a more appropriate definition for nonalcoholic fatty liver disease (NAFLD). Previous studies have shown an association between liver fibrosis scores and cardiovascular disease (CVD) in patients with NAFLD. In this study, we aimed to investigate the relationship between liver fibrosis scores and coronary artery disease (CAD) severity in patients with MAFLD. Methods This study was conducted on 1346 patients with MAFLD at the Second Hospital of Dalian Medical University between January 2018 and December 2021. We calculated the liver fibrosis scores, including the fibrosis 4 (FIB-4) score, nonalcoholic fatty liver disease fibrosis score (NFS), and aspartate aminotransferase-to-platelet ratio index (APRI). We divided the participants into three groups based on the degree of coronary artery stenosis assessed using coronary computed tomography angiography (CCTA): CAD (≥50%), non-obstructive (1-49%), and normal (no stenosis). Results An increased FIB-4 score and NFS were significantly associated with CAD severity in patients with MAFLD. The percentage of patients with a high FIB-4 score was higher in the CAD group than in the other two groups (5.80%, 4.31%, and 2.24%, respectively; p<0.001), as was the percentage of patients with NFS (11.12%, 5.19%, and 0.93%, respectively; p<0.001). Carotid atherosclerosis, creatinine levels, and CAC scores were significant predictors of CAD. The FIB-4 score and NFS were independently associated with CAD even after adjusting for sex and well-known cardiovascular risk factors. The APRI was not a significant factor for CAD in any model. In the bivariate correlation analysis, the FIB-4 score and NFS were directly correlated with CAC scores. Conclusion Non-invasive liver fibrosis scores (FIB-4 and NFS) were significantly associated with the CAD severity and CAC scores in patients with MAFLD. Screening for CAD may be beneficial for subjects with high liver fibrosis risk MAFLD.
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Affiliation(s)
- Chuan Lu
- Department of Cardiology, The Second Hospital of Dalian Medical University, Dalian, 116023, People’s Republic of China
| | - Yan Chen
- Department of Cardiology, The Second Hospital of Dalian Medical University, Dalian, 116023, People’s Republic of China
| | - Yue Zhang
- Department of Gastroenterology, The Second Hospital of Dalian Medical University, Dalian, 116023, People’s Republic of China
| | - Xin Zhao
- Department of Cardiology, The Second Hospital of Dalian Medical University, Dalian, 116023, People’s Republic of China
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12
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Curci R, Bianco A, Franco I, Bonfiglio C, Campanella A, Mirizzi A, Giannuzzi V, Cozzolongo R, Veronese N, Osella AR. Lifestyle Modification: Evaluation of the Effects of Physical Activity and Low-Glycemic-Index Mediterranean Diet on Fibrosis Score. Nutrients 2023; 15:3520. [PMID: 37630711 PMCID: PMC10459797 DOI: 10.3390/nu15163520] [Citation(s) in RCA: 2] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/18/2023] [Revised: 08/03/2023] [Accepted: 08/08/2023] [Indexed: 08/27/2023] Open
Abstract
BACKGROUND Non-Alcoholic Fatty Liver Disease (NAFLD) is one the most prevalent causes of chronic liver disease worldwide. In the absence of an approved drug treatment, lifestyle modification is the first intervention strategy. This study aimed to estimate the main effect of two different physical activity (PA) programs, and a Low-Glycemic-Index Mediterranean Diet (LGIMD), or their combined effect on liver fibrosis parameters in subjects with NAFLD. METHODS Subjects with moderate or severe NAFLD grade of severity (n = 144) were randomly assigned to six intervention arms for three months: LGIMD, PA programs, and their combination. Data were collected at baseline, 45 days, and 90 days. Transient elastography was performed to assess the outcome. RESULTS at 90 days, a statistically significant reduction in kPa was found among subjects following LGMID (-2.85, 95% CI -5.24, -0.45) and those following an LGIMD plus PA1 (-2.37, 95% CI -4.39, -0.35) and LGIMD plus Pa2 (-2.21, 95% CI -4.10, -0.32). The contrast between time 2 and time 1 of the LGIMD plus PA2 treatment showed a statistically significant increase, and vice versa: the contrast between time 3 and time 2 of the same treatment showed a statistically significant reduction. The PA1 and PA2 arms also showed reduced kPa, although the results did not reach statistical significance. CONCLUSIONS The intervention arms, LGIMD, LGIMD+PA1, and LGIMD+PA2, reduced the fibrosis score.
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Affiliation(s)
- Ritanna Curci
- Laboratory of Epidemiology and Statistics, National Institute of Gastroenterology—IRCCS “S. de Bellis”, Via Turi, 70013 Castellana Grotte, Italy; (R.C.); (A.B.); (I.F.); (C.B.); (A.C.)
| | - Antonella Bianco
- Laboratory of Epidemiology and Statistics, National Institute of Gastroenterology—IRCCS “S. de Bellis”, Via Turi, 70013 Castellana Grotte, Italy; (R.C.); (A.B.); (I.F.); (C.B.); (A.C.)
| | - Isabella Franco
- Laboratory of Epidemiology and Statistics, National Institute of Gastroenterology—IRCCS “S. de Bellis”, Via Turi, 70013 Castellana Grotte, Italy; (R.C.); (A.B.); (I.F.); (C.B.); (A.C.)
| | - Caterina Bonfiglio
- Laboratory of Epidemiology and Statistics, National Institute of Gastroenterology—IRCCS “S. de Bellis”, Via Turi, 70013 Castellana Grotte, Italy; (R.C.); (A.B.); (I.F.); (C.B.); (A.C.)
| | - Angelo Campanella
- Laboratory of Epidemiology and Statistics, National Institute of Gastroenterology—IRCCS “S. de Bellis”, Via Turi, 70013 Castellana Grotte, Italy; (R.C.); (A.B.); (I.F.); (C.B.); (A.C.)
| | | | - Vito Giannuzzi
- Gastroenterology Unit, National Institute of Gastroenterology—IRCCS “S. de Bellis”, Via Turi, 70013 Castellana Grotte, Italy; (V.G.); (R.C.)
| | - Raffaele Cozzolongo
- Gastroenterology Unit, National Institute of Gastroenterology—IRCCS “S. de Bellis”, Via Turi, 70013 Castellana Grotte, Italy; (V.G.); (R.C.)
| | - Nicola Veronese
- Geriatric Unit, Department of Medicine, University of Palermo, 90100 Palermo, Italy;
| | - Alberto Ruben Osella
- Laboratory of Epidemiology and Statistics, National Institute of Gastroenterology—IRCCS “S. de Bellis”, Via Turi, 70013 Castellana Grotte, Italy; (R.C.); (A.B.); (I.F.); (C.B.); (A.C.)
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13
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Urias E, Chen VL. Screening for At-Risk Nonalcoholic Fatty Liver Disease in the Primary Care Setting. Semin Liver Dis 2023; 43:133-141. [PMID: 37105224 PMCID: PMC10668862 DOI: 10.1055/a-2082-5203] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 04/29/2023]
Abstract
While nonalcoholic fatty liver disease is a leading cause of end-stage liver disease, most patients with nonalcoholic fatty liver disease do not develop cirrhosis and its complications. Therefore, risk stratification using inexpensive, noninvasive screening modalities is critical to avoid overdiagnosis and overtreatment of a large proportion of the population. In this review, we discuss the data supporting screening and current professional society recommendations on this topic. Screening for at-risk nonalcoholic fatty liver disease is recommended in patients with risk factors including diabetes, the metabolic syndrome, hepatic steatosis, and elevated aminotransferases. Screening typically consists of noninvasive testing using serum biomarkers followed by elastography using specialized imaging modalities. This sequential screening approach accurately identifies both high- and low-risk patients and is cost-effective when applied to at-risk populations. In conclusion, screening for advanced nonalcoholic fatty liver disease in the primary care setting is a crucial part of identifying high-risk patients who may benefit from aggressive intervention while avoiding overtreatment of patients at low risk of liver-related complications.
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Affiliation(s)
- Esteban Urias
- Department of Internal Medicine, University of Michigan, Ann Arbor, Michigan
| | - Vincent L Chen
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, University of Michigan, Ann Arbor, Michigan
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14
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Side effect profile of pharmacologic therapies for liver fibrosis in nonalcoholic fatty liver disease: a systematic review and network meta-analysis. Eur J Gastroenterol Hepatol 2023; 35:1-14. [PMID: 36468565 DOI: 10.1097/meg.0000000000002471] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/10/2022]
Abstract
Several studies have found that antifibrosis treatment for nonalcoholic fatty liver disease (NAFLD) can cause a variety of side effects. No network meta-analysis (NMA) analyzes the adverse events of antifibrotic drugs for NAFLD. This NMA aimed to systematically compare the drug-related side effects when using different pharmacological agents for the treatment of liver fibrosis in NAFLD. PubMed, EMBASE, Web of Science and Cochrane Library were systematically searched to select related studies published in English from the database inception until 30 June 2022. We conducted Bayesian fixed-effects NMA using data from randomized controlled trials (RCTs) to derive relative risks (RRs). The surface under the cumulative ranking (SUCRA) probabilities was used to assess ranking. A total of 26 RCTs with 19 interventions met the inclusion criteria. SUCRA analysis suggested that the lanifibranor group had the highest risk of diarrhea (SUCRA, 94), whereas the liraglutide group had the highest risk of constipation (SUCRA, 92.9). The semaglutide group showed the highest incidence of nausea (SUCRA, 81.2) and abdominal pain (SUCRA, 90.5), respectively. The cenicriviroc group showed the highest risk in the incidence of fatigue (SUCRA, 82.4). The MSDC-0602K group had the highest risk of headache (SUCRA, 76.4), whereas the obeticholic acid group had the highest risk of pruritus (SUCRA, 80.1). The risk of side effects significantly varied among different pharmacologic regimens, and evidence showed that lanifibranor, liraglutide, semaglutide, cenicriviroc, MSDC-0602K and obeticholic acid were the pharmacological interventions with the highest risk in patients with NAFLD. This study may guide clinicians and support further research.
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15
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Lee CH. Metabolic dysfunction-associated fatty liver disease - How relevant is this to primary care physicians and diabetologists? Prim Care Diabetes 2022; 16:245-251. [PMID: 35086794 DOI: 10.1016/j.pcd.2022.01.005] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/08/2022] [Revised: 01/18/2022] [Accepted: 01/20/2022] [Indexed: 11/30/2022]
Abstract
Metabolic-dysfunction associated fatty liver disease (MAFLD) is a newly introduced entity hoping to more precisely define fatty liver disease. Despite the controversies surrounding MAFLD, the definition is getting more widely accepted by the global liver-health community. MAFLD represents a cohort of patients enriched with more advanced liver disease, cardio-renal and metabolic complications with increased mortality. This review aims to provide all primary care physicians and diabetologists with a clinical management update from a non-hepatologist's perspective, and a summary of important findings from recent studies to raise disease awareness and highlight the relevance of MAFLD to their daily clinical practice.
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Affiliation(s)
- Chi-Ho Lee
- Department of Medicine, University of Hong Kong, Hong Kong; State Key Laboratory of Pharmaceutical Biotechnology, University of Hong Kong, Hong Kong.
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16
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Tamaki N, Higuchi M, Kurosaki M, Izumi N. Letter: predictive role of magnetic resonance elastography in chronic liver disease-still a long way to go. Authors' reply. Aliment Pharmacol Ther 2022; 55:622-623. [PMID: 35141919 DOI: 10.1111/apt.16791] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/21/2022]
Affiliation(s)
- Nobuharu Tamaki
- Department of Gastroenterology and Hepatology, Musashino Red Cross Hospital, Musashino, Japan.,First Department of Internal Medicine, Faculty of Medicine, University of Yamanashi, Yamanashi, Japan.,NAFLD Research Center, Division of Gastroenterology and Hepatology, Department of Medicine, University of California San Diego, La Jolla, CA, USA
| | - Mayu Higuchi
- Department of Gastroenterology and Hepatology, Musashino Red Cross Hospital, Musashino, Japan.,First Department of Internal Medicine, Faculty of Medicine, University of Yamanashi, Yamanashi, Japan
| | - Masayuki Kurosaki
- Department of Gastroenterology and Hepatology, Musashino Red Cross Hospital, Musashino, Japan
| | - Namiki Izumi
- Department of Gastroenterology and Hepatology, Musashino Red Cross Hospital, Musashino, Japan
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17
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Giri S, Angadi S. Letter: predictive role of magnetic resonance elastography in chronic liver disease - still a long way to go. Aliment Pharmacol Ther 2022; 55:620-621. [PMID: 35141921 DOI: 10.1111/apt.16771] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/22/2022]
Abstract
LINKED CONTENTThis article is linked to Higuchi et al papers. To view these articles, visit https://doi.org/10.1111/apt.16745 and https://doi.org/10.1111/apt.16791
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Affiliation(s)
- Suprabhat Giri
- Department of Gastroenterology, Nizam's Institute of Medical Sciences, Hyderabad, India
| | - Sumaswi Angadi
- Department of Gastroenterology, Nizam's Institute of Medical Sciences, Hyderabad, India
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18
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Abstract
The global prevalence of non‐alcoholic fatty liver disease (NAFLD) is rising, along with the epidemic of diabesity. NAFLD is present in >70% of individuals with type 2 diabetes. Although the mutually detrimental relationship between NAFLD and type 2 diabetes has been well established, a multitude of recent studies have further shown that type 2 diabetes is closely linked to the development of cirrhosis, hepatocellular carcinoma, liver‐related morbidity and mortality. In contrast, NAFLD also negatively impacts type 2 diabetes both in terms of its incidence and related adverse clinical outcomes, including cardiovascular and chronic kidney diseases. In response to these global health threats, clinical care pathways for NAFLD and guidelines for metabolic dysfunction‐associated fatty liver disease have been developed. Several antidiabetic agents have been evaluated for their potential hepatic benefits with promising results. Furthermore, type 2 diabetes patients are increasingly represented in clinical trials of novel therapeutics for NAFLD. However, despite the wealth of knowledge in NAFLD and type 2 diabetes, lack of awareness of the disease and the potential weight of this problem remains a major challenge, especially among clinicians who are outside the field of hepatology and gastroenterology. This review therefore aimed to provide all diabetes care providers with a summary of the latest evidence that supports NAFLD as an emerging diabetic complication of increasing importance, and to present the current recommendations, focusing on the assessment and therapeutic strategies, on the management of NAFLD among type 2 diabetes patients.
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Affiliation(s)
- C H Lee
- Department of Medicine, University of Hong Kong, Hong Kong SAR.,State Key Laboratory of Pharmaceutical Biotechnology, University of Hong Kong, Hong Kong SAR
| | - Dtw Lui
- Department of Medicine, University of Hong Kong, Hong Kong SAR
| | - Ksl Lam
- Department of Medicine, University of Hong Kong, Hong Kong SAR.,State Key Laboratory of Pharmaceutical Biotechnology, University of Hong Kong, Hong Kong SAR
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19
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Vilarinho S, Ajmera V, Zheng M, Loomba R. Emerging Role of Genomic Analysis in Clinical Evaluation of Lean Individuals With NAFLD. Hepatology 2021; 74:2241-2250. [PMID: 34233030 PMCID: PMC8463418 DOI: 10.1002/hep.32047] [Citation(s) in RCA: 60] [Impact Index Per Article: 15.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/08/2021] [Revised: 05/25/2021] [Accepted: 07/01/2021] [Indexed: 12/18/2022]
Abstract
Whereas the rising prevalence of nonalcoholic fatty liver disease (NAFLD) is closely related with the global obesity epidemic, up to 10–20% of individuals with NAFLD are lean as defined by a body mass index of < 25 kg/m2, or < 23 kg/m2 in Asians. This entity designated as “lean NAFLD” is estimated to affect 8 to 10 million individuals in the United States alone. Here, we review the emerging data on the epidemiology, natural history and prognosis of lean NAFLD and put forward a diagnostic approach that combines detailed clinical phenotyping with genomic analysis. We propose two subtypes of lean NAFLD referred to as type 1: individuals with visceral adiposity and insulin resistance but normal BMI; and type 2: lean individuals with hepatic steatosis secondary to a known or unknown monogenic disease. We envision that incorporation of genomic analysis in the diagnostic algorithm of lean patients with NAFLD will elucidate the contribution of common genetic variants through the calculation of NAFLD polygenic risk score and also characterize the diverse array of rare monogenic diseases that can lead to triglyceride accumulation in the cytoplasm of hepatocytes. Collectively, the integration of a molecular diagnosis in the clinical evaluation of patients with lean NAFLD will provide an accurate diagnosis, with possible targeted therapies and may uncover novel molecular mechanisms with potential broader therapeutic implications.
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Affiliation(s)
- Sílvia Vilarinho
- Departments of Internal Medicine, Section of Digestive Diseases, and of Pathology, Yale School of Medicine, New Haven, CT
| | - Veeral Ajmera
- NAFLD Research Center, Division of Gastroenterology. University of California at San Diego, La Jolla, CA, USA
| | - Melanie Zheng
- Departments of Internal Medicine, Section of Digestive Diseases, and of Pathology, Yale School of Medicine, New Haven, CT
| | - Rohit Loomba
- NAFLD Research Center, Division of Gastroenterology. University of California at San Diego, La Jolla, CA, USA
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20
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Delgado GE, Kleber ME, Moissl AP, Yazdani B, Kusnik A, Ebert MP, März W, Krämer BK, Lammert A, Teufel A. Surrogate scores of advanced fibrosis in NAFLD/NASH do not predict mortality in patients with medium-to-high cardiovascular risk. Am J Physiol Gastrointest Liver Physiol 2021; 321:G252-G261. [PMID: 34132110 DOI: 10.1152/ajpgi.00058.2021] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 01/31/2023]
Abstract
Untreated non-alcoholic fatty liver disease (NAFLD) may have significant consequences including an increase in mortality and cardiovascular injury. Thus, early detection of NAFLD is currently believed not only to prevent liver-related but also cardiovascular mortality. However, almost nothing is known about coexisting NAFLD in patients with coronary artery disease (CAD). We investigated the impact of surrogate scores of fibrosis in NAFLD in a large cohort of patients referred to coronary angiography. Modeling the common NALFD and fibrosis scores, fibrosis-4 index (FIB-4) and NAFLD fibrosis score (NFS), as splines revealed significant associations with all-cause and cardiovascular mortality when Cox regression models were only adjusted for cardiovascular risk factors that were not already included in the calculation of the scores. Stratifying the scores into quartiles yielded hazard ratios [95% confidence interval (CI)] for all-cause and cardiovascular mortality for the 4th quartile versus the 1st quartile of 2.28 (1.90-2.75) and 2.11 (1.67-2.67) for FIB-4 and of 3.21 (2.61-3.94) and 3.12 (2.41-4.04) for NFS. However, we did not observe an independent association of FIB-4 or NFS with overall or cardiovascular mortality in our prospective CAD cohort after full adjustment for all cardiovascular risk factors [all-cause mortality: HR 1.13 (0.904-1.41) and 1.17 (0.903-1.52); cardiovascular mortality: HR 1.06 (0.8-1.41) and 1.02 (0.738-1.41)]. Thus, neither FIB-4 nor NFS, as surrogate markers for NAFLD/NASH, were independent risk factors for overall or cardiovascular mortality in patients with CAD. Our data show that surrogate risk scores for NAFLD-related fibrosis do not add information in assessing the CVD events in patients with CAD proven by angiography.NEW & NOTEWORTHY We investigated the impact of NAFLD surrogate markers in a large cohort of patients that had been referred to coronary angiography. In contrast to a repeatedly demonstrated increased link of cardiovascular events in patients with NALFD, we demonstrated that NAFLD surrogate markers were not independent risk factors for overall or cardiovascular mortality in patients with CAD. Thus, these markers may not be useful for primary prevention of cardiovascular events in patients with CAD.
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Affiliation(s)
- Graciela E Delgado
- Department of Medicine V, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
| | - Marcus E Kleber
- Department of Medicine V, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.,SYNLAB MVZ Humangenetik Mannheim GmbH, Mannheim, Germany
| | - Angela P Moissl
- Department of Medicine V, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.,Institute of Nutritional Sciences, Friedrich Schiller University Jena, Jena, Germany.,Competence Cluster for Nutrition and Cardiovascular Health (nutriCARD), Halle-Jena-Leipzig, Germany
| | - Babak Yazdani
- Department of Medicine V, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
| | - Alexander Kusnik
- Department of Medicine II, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.,Clinical Cooperation Unit Healthy Metabolism, Center for Preventive Medicine and Digital Health Baden-Württemberg (CPDBW), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
| | - Matthias P Ebert
- Department of Medicine II, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.,Clinical Cooperation Unit Healthy Metabolism, Center for Preventive Medicine and Digital Health Baden-Württemberg (CPDBW), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
| | - Winfried März
- Department of Medicine V, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.,Synlab Academy, SYNLAB Holding Deutschland GmbH, Mannheim and Augsburg, Germany
| | - Bernhard K Krämer
- Department of Medicine V, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.,Clinical Cooperation Unit Healthy Metabolism, Center for Preventive Medicine and Digital Health Baden-Württemberg (CPDBW), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
| | - Alexander Lammert
- Department of Medicine V, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.,Praxis für Stoffwechsel- und Nierenerkrankungen, Zentrum für Dialyse und Apherese, Grünstadt, Germany
| | - Andreas Teufel
- Clinical Cooperation Unit Healthy Metabolism, Center for Preventive Medicine and Digital Health Baden-Württemberg (CPDBW), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.,Department of Medicine II, Section of Hepatology, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
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21
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Chun HS, Lee JS, Lee HW, Kim BK, Park JY, Kim DY, Ahn SH, Lee YH, Kim YD, Kim SU. Association between the severity of liver fibrosis and cardiovascular outcomes in patients with type 2 diabetes. J Gastroenterol Hepatol 2021; 36:1703-1713. [PMID: 33370454 DOI: 10.1111/jgh.15387] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/29/2020] [Revised: 12/07/2020] [Accepted: 12/21/2020] [Indexed: 12/20/2022]
Abstract
BACKGROUND AND AIM Cardiovascular disease (CVD) is the principal cause of death in patients with type 2 diabetes (T2D). In this study, we assessed whether liver fibrosis predicted the risk of CVD in patients with T2D. METHODS A total of 1481 patients who had commenced oral antidiabetic drugs to treat newly diagnosed T2D between 2006 and 2010 were recruited. The fibrosis-4 index (FIB-4), non-alcoholic fatty liver disease fibrosis score (NFS), and BARD score were used to assess fibrotic burden at the time of T2D diagnosis. RESULTS During the follow-up period (median 88.1 [interquartile range 36.6-113.6] months), 242 (16.3%) patients developed CVD. CVD occurred frequently in older patients and was associated with hypertension; metabolic syndrome; obesity; smoking; administration of statin, which is an antihyperlipidemic drug; lower platelet counts; lower alanine aminotransferase, total cholesterol, and HbA1c levels; higher C-peptide and homeostatic model assessment of insulin resistance levels; and higher FIB-4, NFS, and BARD score (all P < 0.05). FIB-4 (hazard ratio [HR] = 1.163), NFS (HR = 1.322), BARD score (HR = 1.564), metabolic syndrome (HR = 1.556), smoking (HR = 2.829), and statin use (HR = 0.603) independently predicted the risk of CVD (all P < 0.05). The cumulative incidence of CVD was significantly different among groups stratified by liver fibrotic burden (all P < 0.05, log-rank test). Competing risk analysis showed a significant association between the severity of liver fibrosis and CVD development (all P < 0.001, Gray's test). CONCLUSIONS The severity of liver fibrosis independently predicted CVD in patients with T2D. Thus, assessment of liver fibrosis might allow physicians to optimize the timing of appropriate cardiovascular interventions in such patients.
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Affiliation(s)
- Ho Soo Chun
- Department of Internal Medicine, Yonsei University College of Medicine, Seoul, Korea
- Institute of Gastroenterology, Yonsei University College of Medicine, Seoul, Korea
| | - Jae Seung Lee
- Department of Internal Medicine, Yonsei University College of Medicine, Seoul, Korea
- Institute of Gastroenterology, Yonsei University College of Medicine, Seoul, Korea
- Yonsei Liver Center, Severance Hospital, Seoul, Korea
| | - Hye Won Lee
- Department of Internal Medicine, Yonsei University College of Medicine, Seoul, Korea
- Institute of Gastroenterology, Yonsei University College of Medicine, Seoul, Korea
- Yonsei Liver Center, Severance Hospital, Seoul, Korea
| | - Beom Kyung Kim
- Department of Internal Medicine, Yonsei University College of Medicine, Seoul, Korea
- Institute of Gastroenterology, Yonsei University College of Medicine, Seoul, Korea
- Yonsei Liver Center, Severance Hospital, Seoul, Korea
| | - Jun Yong Park
- Department of Internal Medicine, Yonsei University College of Medicine, Seoul, Korea
- Institute of Gastroenterology, Yonsei University College of Medicine, Seoul, Korea
- Yonsei Liver Center, Severance Hospital, Seoul, Korea
| | - Do Young Kim
- Department of Internal Medicine, Yonsei University College of Medicine, Seoul, Korea
- Institute of Gastroenterology, Yonsei University College of Medicine, Seoul, Korea
- Yonsei Liver Center, Severance Hospital, Seoul, Korea
| | - Sang Hoon Ahn
- Department of Internal Medicine, Yonsei University College of Medicine, Seoul, Korea
- Institute of Gastroenterology, Yonsei University College of Medicine, Seoul, Korea
- Yonsei Liver Center, Severance Hospital, Seoul, Korea
| | - Yong-Ho Lee
- Department of Internal Medicine, Yonsei University College of Medicine, Seoul, Korea
- Institute of Endocrine Research, Yonsei University College of Medicine, Seoul, Korea
| | - Young Dae Kim
- Department of Neurology, Yonsei University College of Medicine, Seoul, Korea
| | - Seung Up Kim
- Department of Internal Medicine, Yonsei University College of Medicine, Seoul, Korea
- Institute of Gastroenterology, Yonsei University College of Medicine, Seoul, Korea
- Yonsei Liver Center, Severance Hospital, Seoul, Korea
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22
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Park JG, Jung J, Verma KK, Kang MK, Madamba E, Lopez S, Yonan AQ, Liu A, Bettencourt R, Sirlin C, Loomba R. Liver stiffness by magnetic resonance elastography is associated with increased risk of cardiovascular disease in patients with non-alcoholic fatty liver disease. Aliment Pharmacol Ther 2021; 53:1030-1037. [PMID: 33764550 PMCID: PMC8514119 DOI: 10.1111/apt.16324] [Citation(s) in RCA: 27] [Impact Index Per Article: 6.8] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/31/2020] [Revised: 01/30/2021] [Accepted: 02/24/2021] [Indexed: 12/09/2022]
Abstract
BACKGROUND Magnetic resonance elastography (MRE) is a reliable non-invasive alternative to liver biopsy for assessing liver fibrosis. There are limited data regarding an association between liver fibrosis by MRE and risk of cardiovascular disease (CVD). AIM To investigate the association of high-risk CVD phenotype determined by coronary artery calcification (CAC) with liver fibrosis by MRE in patients with non-alcoholic fatty liver disease (NAFLD). METHOD This was a cross-sectional analysis of well-characterised, prospective cohorts including 105 patients with NAFLD (MR imaging-derived proton density fat fraction ≥ 5%) with contemporaneous cardiac computed tomography (CT) and MRE. Patients were assessed using MRE for liver stiffness, and cardiac CT for the presence of CAC (defined as coronary artery calcium score > 0). Odds of presence of CAC were analysed using logistic regression analysis. RESULTS The average age and body mass index were 54.9 years and 32.9 kg/m2 respectively. In this cohort, 49.5% of patients had CAC and 35.2% had significant liver fibrosis (defined as MRE ≥2.97 kPa). Compared to patients without CAC, those with CAC were older (50.0 [39.0-59.0] vs 63.0 [55.5-67.5], P < 0.001) and had higher Framingham risk score (FRS, 1.0 [0.5-3.5] vs 6.0 [2.0-12.0], P < 0.001). In multivariable-adjusted analysis, liver stiffness as a continuous trait on MRE was independently associated with the presence of CAC in a sex and age-adjusted model (adjusted odd ratios [aOR] = 2.23, 95% confidence interval [CI] = 1.31-4.34, P = 0.007) as well as in a FRS-adjusted model (aOR = 2.16, 95% CI = 1.29-4.09, P = 0.008). When analysed as a dichotomous trait, significant fibrosis (MRE-stiffness ≥2.97 kPa) remained independently associated with the presence of CAC in both FRS-adjusted model and sex and age-adjusted model (aOR = 3.21-3.53, P = 0.013-0.017). In addition, CAC was more prevalent in patients with significant fibrosis than those without as determined by MRE (67.6% vs 39.7%, P = 0.012). CONCLUSION Liver stiffness determined by MRE is an independent predictor for the presence of CAC in patients with NAFLD. Patients with NAFLD and significant fibrosis by MRE should be considered for further cardiovascular risk assessment, regardless of their FRS.
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Affiliation(s)
- Jung Gil Park
- NAFLD Research Center, Division of Gastroenterology and Hepatology, Department of Medicine, University of California at San Diego, La Jolla, United States,Department of Internal Medicine, College of Medicine, Yeungnam University, Daegu, South Korea
| | - Jinho Jung
- NAFLD Research Center, Division of Gastroenterology and Hepatology, Department of Medicine, University of California at San Diego, La Jolla, United States
| | - Kritin K Verma
- NAFLD Research Center, Division of Gastroenterology and Hepatology, Department of Medicine, University of California at San Diego, La Jolla, United States
| | - Min Kyu Kang
- Department of Internal Medicine, College of Medicine, Yeungnam University, Daegu, South Korea
| | - Egbert Madamba
- NAFLD Research Center, Division of Gastroenterology and Hepatology, Department of Medicine, University of California at San Diego, La Jolla, United States
| | - Scarlett Lopez
- NAFLD Research Center, Division of Gastroenterology and Hepatology, Department of Medicine, University of California at San Diego, La Jolla, United States
| | - Aed Qas Yonan
- NAFLD Research Center, Division of Gastroenterology and Hepatology, Department of Medicine, University of California at San Diego, La Jolla, United States
| | - Amy Liu
- NAFLD Research Center, Division of Gastroenterology and Hepatology, Department of Medicine, University of California at San Diego, La Jolla, United States
| | - Ricki Bettencourt
- NAFLD Research Center, Division of Gastroenterology and Hepatology, Department of Medicine, University of California at San Diego, La Jolla, United States
| | - Claude Sirlin
- University of California at San Diego, Liver Imaging Group, Department of Radiology, La Jolla, United States
| | - Rohit Loomba
- NAFLD Research Center, Division of Gastroenterology and Hepatology, Department of Medicine, University of California at San Diego, La Jolla, United States,University of California at San Diego, Department of Family Medicine and Public Health, La Jolla, United States
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23
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Abstract
PURPOSE OF REVIEW Nonalcoholic fatty liver disease (NAFLD) and type 2 diabetes mellitus (T2DM) are strongly associated. Both also associate with an increased risk of cardiovascular disease (CVD). RECENT FINDINGS Several studies have provided evidence that NAFLD could be an independent CVD risk factor. Given the strong association between NAFLD and T2DM, assessing the independent CV effect of these two conditions remains challenging. However, patients with T2DM and NAFLD exhibit higher risk of CVD compared with T2DM without NAFLD suggesting a potential synergistic increase of CV risk in patients with both T2DM and NAFLD supported by several shared pathophysiological pathways. Several anti-diabetic therapies have shown beneficial effect on both NAFLD and CVD. Patients with T2DM and NAFLD should be considered at high risk of CVD and could benefit from more intensive CV prevention. Additional long-term follow-up is needed to demonstrate that the treatment of NAFLD effectively reduces the risk of CVD.
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Affiliation(s)
- Cyrielle Caussy
- Hôpital Lyon Sud, Département Endocrinologie, Diabète et Nutrition, Hospices Civils de Lyon, 69495, Pierre-Bénite, France.
| | - Adrien Aubin
- Hôpital Lyon Sud, Département Endocrinologie, Diabète et Nutrition, Hospices Civils de Lyon, 69495, Pierre-Bénite, France
| | - Rohit Loomba
- Department of Medicine, NAFLD Research Center, University of California at San Diego, La Jolla, CA, USA.
- Division of Gastroenterology, Department of Medicine, University of California at San Diego, La Jolla, CA, USA.
- Division of Epidemiology, Department of Family and Preventive Medicine, University of California at San Diego, La Jolla, CA, USA.
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24
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Shroff H, VanWagner LB. Cardiovascular Disease in Nonalcoholic Steatohepatitis: Screening and Management. ACTA ACUST UNITED AC 2021; 19:315-326. [PMID: 33585157 DOI: 10.1007/s11901-020-00530-0] [Citation(s) in RCA: 16] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/13/2022]
Abstract
Purpose of Review The global burden of non-alcoholic steatohepatitis (NASH) as a major cause of chronic liver disease continues to rise. Cardiovascular disease (CVD) is a leading cause of morbidity and mortality in this patient population. The current review summarizes recent advances in the understanding of CVD in NASH and strategies for screening and management. Recent findings Large genetic epidemiological studies support the intricate role of the metabolic syndrome in the pathophysiology of CVD risk in patients with NASH. Atherosclerotic CVD risk scores can predict elevated CV risk in NASH, but additional work is necessary to refine risk stratification and to guide optimal management. New antidiabetic agents may offer benefit in treating steatosis and reducing CV morbidity in NASH. Summary Achieving improved outcomes in patients with NASH requires that future efforts focus on optimizing methods for CVD screening and designing clinical trials with long-term cardiovascular endpoints in mind.
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Affiliation(s)
- Hersh Shroff
- Division of Gastroenterology and Hepatology, Department of Medicine
| | - Lisa B VanWagner
- Division of Gastroenterology and Hepatology, Department of Medicine.,Department of Preventive Medicine, Northwestern University Feinberg School of Medicine, Chicago, IL
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25
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Ichikawa K, Miyoshi T, Osawa K, Miki T, Toda H, Ejiri K, Yoshida M, Nanba Y, Yoshida M, Nakamura K, Morita H, Ito H. Prognostic value of non-alcoholic fatty liver disease for predicting cardiovascular events in patients with diabetes mellitus with suspected coronary artery disease: a prospective cohort study. Cardiovasc Diabetol 2021; 20:8. [PMID: 33413363 PMCID: PMC7791695 DOI: 10.1186/s12933-020-01192-4] [Citation(s) in RCA: 35] [Impact Index Per Article: 8.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/11/2020] [Accepted: 12/09/2020] [Indexed: 12/14/2022] Open
Abstract
Background Risk stratification of cardiovascular events in patients with type 2 diabetes mellitus (T2DM) has not been established. Coronary artery calcium score (CACS) and non-alcoholic fatty liver disease (NAFLD) are independently associated with cardiovascular events in T2DM patients. This study examined the incremental prognostic value of NAFLD assessed by non-enhanced computed tomography (CT) in addition to CACS and Framingham risk score (FRS) for cardiovascular events in T2DM patients. Methods This prospective pilot study included 529 T2DM outpatients with no history of cardiovascular disease who underwent CACS measurement because of suspected coronary artery disease. NAFLD was defined on CT images as a liver:spleen attenuation ratio < 1.0. Cardiovascular events were defined as cardiovascular death, nonfatal myocardial infarction, late coronary revascularization, nonfatal stroke, or hospitalization for heart failure. Results Among 529 patients (61% men, mean age 65 years), NAFLD was identified in 143 (27%). Forty-four cardiovascular events were documented during a median follow-up of 4.4 years. In multivariate Cox regression analysis, NAFLD, CACS, and FRS were associated with cardiovascular events (hazard ratios and 95% confidence intervals 5.43, 2.82–10.44, p < 0.001; 1.56, 1.32–1.86, p < 0.001; 1.23, 1.08–1.39, p = 0.001, respectively). The global χ2 score for predicting cardiovascular events increased significantly from 27.0 to 49.7 by adding NAFLD to CACS and FRS (p < 0.001). The addition of NAFLD to a model including CACS and FRS significantly increased the C-statistic from 0.71 to 0.80 (p = 0.005). The net reclassification achieved by adding CACS and FRS was 0.551 (p < 0.001). Conclusions NAFLD assessed by CT, in addition to CACS and FRS, could be useful for identifying T2DM patients at higher risk of cardiovascular events.
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Affiliation(s)
- Keishi Ichikawa
- Department of Cardiovascular Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Graduate School of Medicine, 2-5-1 Shikata-cho, Kita-ku, Okayama, 700-8558, Japan
| | - Toru Miyoshi
- Department of Cardiovascular Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Graduate School of Medicine, 2-5-1 Shikata-cho, Kita-ku, Okayama, 700-8558, Japan.
| | - Kazuhiro Osawa
- Department of Cardiovascular Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Graduate School of Medicine, 2-5-1 Shikata-cho, Kita-ku, Okayama, 700-8558, Japan.,Department of Cardiovascular Medicine, Japanese Red Cross Okayama Hospital, Okayama, Japan
| | - Takashi Miki
- Department of Cardiovascular Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Graduate School of Medicine, 2-5-1 Shikata-cho, Kita-ku, Okayama, 700-8558, Japan
| | - Hironobu Toda
- Department of Cardiovascular Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Graduate School of Medicine, 2-5-1 Shikata-cho, Kita-ku, Okayama, 700-8558, Japan
| | - Kentaro Ejiri
- Department of Cardiovascular Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Graduate School of Medicine, 2-5-1 Shikata-cho, Kita-ku, Okayama, 700-8558, Japan
| | - Masatoki Yoshida
- Department of Cardiovascular Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Graduate School of Medicine, 2-5-1 Shikata-cho, Kita-ku, Okayama, 700-8558, Japan
| | - Yusuke Nanba
- Department of Cardiovascular Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Graduate School of Medicine, 2-5-1 Shikata-cho, Kita-ku, Okayama, 700-8558, Japan
| | - Masashi Yoshida
- Department of Cardiovascular Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Graduate School of Medicine, 2-5-1 Shikata-cho, Kita-ku, Okayama, 700-8558, Japan
| | - Kazufumi Nakamura
- Department of Cardiovascular Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Graduate School of Medicine, 2-5-1 Shikata-cho, Kita-ku, Okayama, 700-8558, Japan
| | - Hiroshi Morita
- Department of Cardiovascular Therapeutics, Dentistry, and Pharmaceutical Sciences, Okayama University Graduate School of Medicine, Okayama, Japan
| | - Hiroshi Ito
- Department of Cardiovascular Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Graduate School of Medicine, 2-5-1 Shikata-cho, Kita-ku, Okayama, 700-8558, Japan
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26
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Thomaides-Brears HB, Lepe R, Banerjee R, Duncker C. Multiparametric MR mapping in clinical decision-making for diffuse liver disease. Abdom Radiol (NY) 2020; 45:3507-3522. [PMID: 32761254 PMCID: PMC7593302 DOI: 10.1007/s00261-020-02684-3] [Citation(s) in RCA: 28] [Impact Index Per Article: 5.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/27/2020] [Revised: 06/12/2020] [Accepted: 07/22/2020] [Indexed: 02/07/2023]
Abstract
Accurate diagnosis, monitoring and treatment decisions in patients with chronic liver disease currently rely on biopsy as the diagnostic gold standard, and this has constrained early detection and management of diseases that are both varied and can be concurrent. Recent developments in multiparametric magnetic resonance imaging (mpMRI) suggest real potential to bridge the diagnostic gap between non-specific blood-based biomarkers and invasive and variable histological diagnosis. This has implications for the clinical care and treatment pathway in a number of chronic liver diseases, such as haemochromatosis, steatohepatitis and autoimmune or viral hepatitis. Here we review the relevant MRI techniques in clinical use and their limitations and describe recent potential applications in various liver diseases. We exemplify case studies that highlight how these techniques can improve clinical practice. These techniques could allow clinicians to increase their arsenals available to utilise on patients and direct appropriate treatments.
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Affiliation(s)
| | - Rita Lepe
- Texas Liver Institute, 607 Camden St, Suite 101, San Antonio, TX, 78215, USA
| | | | - Carlos Duncker
- Perspectum, 600 N. Pearl St. Suite 1960, Plaza of The Americas, Dallas, TX, 75201, USA
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27
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Campos-Murguía A, Ruiz-Margáin A, González-Regueiro JA, Macías-Rodríguez RU. Clinical assessment and management of liver fibrosis in non-alcoholic fatty liver disease. World J Gastroenterol 2020; 26:5919-5943. [PMID: 33132645 PMCID: PMC7584064 DOI: 10.3748/wjg.v26.i39.5919] [Citation(s) in RCA: 29] [Impact Index Per Article: 5.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/15/2020] [Revised: 05/24/2020] [Accepted: 09/22/2020] [Indexed: 02/06/2023] Open
Abstract
Non-alcoholic fatty liver disease (NAFLD) is among the most frequent etiologies of cirrhosis worldwide, and it is associated with features of metabolic syndrome; the key factor influencing its prognosis is the progression of liver fibrosis. This review aimed to propose a practical and stepwise approach to the evaluation and management of liver fibrosis in patients with NAFLD, analyzing the currently available literature. In the assessment of NAFLD patients, it is important to identify clinical, genetic, and environmental determinants of fibrosis development and its progression. To properly detect fibrosis, it is important to take into account the available methods and their supporting scientific evidence to guide the approach and the sequential selection of the best available biochemical scores, followed by a complementary imaging study (transient elastography, magnetic resonance elastography or acoustic radiation force impulse) and finally a liver biopsy, when needed. To help with the selection of the most appropriate method a Fagan's nomogram analysis is provided in this review, describing the diagnostic yield of each method and their post-test probability of detecting liver fibrosis. Finally, treatment should always include diet and exercise, as well as controlling the components of the metabolic syndrome, +/- vitamin E, considering the presence of sleep apnea, and when available, allocate those patients with advanced fibrosis or high risk of progression into clinical trials. The final end of this approach should be to establish an opportune diagnosis and treatment of liver fibrosis in patients with NAFLD, aiming to decrease/stop its progression and improve their prognosis.
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Affiliation(s)
- Alejandro Campos-Murguía
- Department of Gastroenterology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City 14080, Mexico
| | - Astrid Ruiz-Margáin
- Department of Gastroenterology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City 14080, Mexico
| | - José A González-Regueiro
- Department of Gastroenterology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City 14080, Mexico
| | - Ricardo U Macías-Rodríguez
- Department of Gastroenterology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City 14080, Mexico
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28
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Altamirano J, Qi Q, Choudhry S, Abdallah M, Singal AK, Humar A, Bataller R, Borhani AA, Duarte-Rojo A. Non-invasive diagnosis: non-alcoholic fatty liver disease and alcoholic liver disease. Transl Gastroenterol Hepatol 2020; 5:31. [PMID: 32258535 DOI: 10.21037/tgh.2019.11.14] [Citation(s) in RCA: 24] [Impact Index Per Article: 4.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/10/2019] [Accepted: 10/30/2019] [Indexed: 12/18/2022] Open
Abstract
Non-alcoholic fatty liver disease (NAFLD) and alcoholic liver disease (ALD) are becoming the leading causes of chronic liver disease worldwide, significantly impacting public health and healthcare cost. The development of fibrosis is the main factor leading to early mortality and morbidity in NAFLD and ALD. Thus, it is important to timely and reliably evaluate these diseases at early stages, when fibrosis is not advanced or when steatosis predominates. Liver biopsy has been the standard of reference for fibrosis and steatosis, however, its invasiveness precludes its widespread use. There is growing research on non-invasive methods for diagnosing and stratifying fibrosis and steatosis in NAFLD and ALD. This review presents clinical evidence on the use of non-invasive assessment of liver disease (blood-based and imaging-based) in patients with NALFD and ALD, and proposes algorithms incorporating these tests into their management.
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Affiliation(s)
- Jose Altamirano
- Department of Internal Medicine (Hepatology Section), Hospital Quironsalud Barcelona, Spain
| | - Qiaochu Qi
- Department of Medicine, University of Pittsburgh, Pittsburgh, PA, USA
| | - Sabina Choudhry
- Department of Radiology, University of South Dakota, Vermillion, SD, USA
| | - Mohamed Abdallah
- Department of Internal Medicine (Hepatology Section), University of South Dakota, Vermillion, SD, USA
| | - Ashwani K Singal
- Department of Medicine, University of South Dakota Sanford School of Medicine, Avera McKennan University Hospital Transplant Hepatology, Sioux Falls, SD, USA
| | - Abhinav Humar
- Starzl Transplantation Institute, University of Pittsburgh, Pittsburgh, PA, USA
| | - Ramón Bataller
- Starzl Transplantation Institute, University of Pittsburgh, Pittsburgh, PA, USA.,Division of Gastroenterology and Hepatology, University of Pittsburgh, Pittsburgh, PA, USA
| | - Amir Ali Borhani
- Department of Radiology, University of Pittsburgh, Pittsburgh, PA, USA
| | - Andrés Duarte-Rojo
- Starzl Transplantation Institute, University of Pittsburgh, Pittsburgh, PA, USA.,Division of Gastroenterology and Hepatology, University of Pittsburgh, Pittsburgh, PA, USA
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Ballestri S, Tana C, Di Girolamo M, Fontana MC, Capitelli M, Lonardo A, Cioni G. Semi-Quantitative Ultrasonographic Evaluation of NAFLD. Curr Pharm Des 2020; 26:3915-3927. [PMID: 32303161 DOI: 10.2174/1381612826666200417142444] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/10/2019] [Accepted: 03/20/2020] [Indexed: 02/07/2023]
Abstract
Nonalcoholic fatty liver disease (NAFLD) embraces histopathological entities ranging from the relatively benign simple steatosis to the progressive form nonalcoholic steatohepatitis (NASH), which is associated with fibrosis and an increased risk of progression to cirrhosis and hepatocellular carcinoma. NAFLD is the most common liver disease and is associated with extrahepatic comorbidities including a major cardiovascular disease burden. The non-invasive diagnosis of NAFLD and the identification of subjects at risk of progressive liver disease and cardio-metabolic complications are key in implementing personalized treatment schedules and follow-up strategies. In this review, we highlight the potential role of ultrasound semiquantitative scores for detecting and assessing steatosis severity, progression of NAFLD, and cardio-metabolic risk. Ultrasonographic scores of fatty liver severity act as sensors of cardio-metabolic health and may assist in selecting patients to submit to second-line non-invasive imaging techniques and/or liver biopsy.
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Affiliation(s)
- Stefano Ballestri
- Internal Medicine Unit, Pavullo Hospital, Azienda USL, Modena, Italy
| | - Claudio Tana
- Internal Medicine Unit, Pavullo Hospital, Azienda USL, Modena, Italy
| | - Maria Di Girolamo
- Internal Medicine Unit, Pavullo Hospital, Azienda USL, Modena, Italy
| | | | - Mariano Capitelli
- Internal Medicine Unit, Pavullo Hospital, Azienda USL, Modena, Italy
| | - Amedeo Lonardo
- Internal Medicine Unit, Pavullo Hospital, Azienda USL, Modena, Italy
| | - Giorgio Cioni
- Internal Medicine Unit, Pavullo Hospital, Azienda USL, Modena, Italy
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30
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Unger LW, Forstner B, Muckenhuber M, Scheuba K, Eigenbauer E, Scheiner B, Pfisterer N, Paternostro R, Trauner M, Mandorfer M, Reiberger T. Hepatic Steatosis in Lean Patients: Risk Factors and Impact on Mortality. Dig Dis Sci 2020; 65:2712-2718. [PMID: 31875288 PMCID: PMC7419366 DOI: 10.1007/s10620-019-06000-y] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/27/2019] [Accepted: 12/05/2019] [Indexed: 12/20/2022]
Abstract
BACKGROUND The prognostic impact of liver steatosis in obese patients is well established. Limited data on the risk factors for and impact of hepatic steatosis in lean patients are available. AIMS Assess risk factors for liver steatosis in lean patients and investigate its impact on survival. METHODS Patients without viral hepatitis and with a BMI ≤ 25 kg/m2 undergoing liver stiffness measurement (LSM) and controlled attenuation parameter (CAP) by transient elastography were retrospectively identified. Clinical characteristics and laboratory test results were obtained at the time of LSM/CAP measurement. National death registry data were obtained in order to assess survival. RESULTS Among n = 218 lean patients, n = 97 (34.5%) showed significant liver steatosis (CAP ≥ 268 dB/m), while n = 184 (65.5%) had no or just mild steatosis (CAP < 268 dB/m). Patients with steatosis had higher GGT (238.0(± 450.3) vs. 112.1(± 180.0) IU/mL; p = 0.013), AST (63(± 67.4) vs. 38.5(± 32.9) IU/mL; p = 0.001), ALT (59.1(± 58.8) vs. 44.3(± 52.7) IU/mL; p = 0.048) and triglyceride levels (120.1(± 80.3) vs. 96.1(± 58.2) mg/dL; p = 0.014), and showed a trend toward more severe fibrosis (LSM 15.6(± 19.5) vs. 12.0(± 15.7) kPa; p = 0.115). In multivariate binary logistic regression analysis, only serum uric acid levels were independently associated with liver steatosis (odds ratio 1.43 per unit mg/dL; 95% CI 1.001-2.054; p = 0.049). During a mean follow-up of 38.9(± 10.6) months, n = 14 patients (5.0%) died. In the absence of advanced fibrosis, survival after 1 year was similar in patients without (98.7%) and with (98.6%) significant steatosis. Patients with advanced fibrosis had worse 1-year survival without concomitant significant steatosis (84.8%) than patients with steatosis (95.8%; log-rank p < 0.001). CONCLUSIONS High serum uric acid levels increase the risk of liver steatosis in lean patients. Liver fibrosis but not hepatic steatosis is a risk factor for impaired survival in lean patients.
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Affiliation(s)
- Lukas W Unger
- Division of General Surgery, Department of Surgery, Medical University of Vienna, Währinger Gürtel 18-20, Vienna, Austria
- Vienna Hepatic Hemodynamic Laboratory, Medical University of Vienna, Währinger Gürtel 18-20, Vienna, Austria
| | - Bernadette Forstner
- Division of General Surgery, Department of Surgery, Medical University of Vienna, Währinger Gürtel 18-20, Vienna, Austria
| | - Moritz Muckenhuber
- Division of General Surgery, Department of Surgery, Medical University of Vienna, Währinger Gürtel 18-20, Vienna, Austria
| | - Katharina Scheuba
- Division of General Surgery, Department of Surgery, Medical University of Vienna, Währinger Gürtel 18-20, Vienna, Austria
| | - Ernst Eigenbauer
- IT-Systems and Communications, Medical University of Vienna, Währinger Gürtel 18-20, Vienna, Austria
| | - Bernhard Scheiner
- Vienna Hepatic Hemodynamic Laboratory, Medical University of Vienna, Währinger Gürtel 18-20, Vienna, Austria
- Division of Gastroenterology and Hepatology, Department of Internal Medicine III, Medical University of Vienna, Währinger Gürtel 18-20, 1090, Vienna, Austria
| | - Nikolaus Pfisterer
- Vienna Hepatic Hemodynamic Laboratory, Medical University of Vienna, Währinger Gürtel 18-20, Vienna, Austria
- Krankenanstalt Rudolfstiftung, Krankenanstaltenverbund Wien (KAV), Vienna, Austria
| | - Rafael Paternostro
- Vienna Hepatic Hemodynamic Laboratory, Medical University of Vienna, Währinger Gürtel 18-20, Vienna, Austria
- Division of Gastroenterology and Hepatology, Department of Internal Medicine III, Medical University of Vienna, Währinger Gürtel 18-20, 1090, Vienna, Austria
| | - Michael Trauner
- Division of Gastroenterology and Hepatology, Department of Internal Medicine III, Medical University of Vienna, Währinger Gürtel 18-20, 1090, Vienna, Austria
| | - Mattias Mandorfer
- Vienna Hepatic Hemodynamic Laboratory, Medical University of Vienna, Währinger Gürtel 18-20, Vienna, Austria
- Division of Gastroenterology and Hepatology, Department of Internal Medicine III, Medical University of Vienna, Währinger Gürtel 18-20, 1090, Vienna, Austria
| | - Thomas Reiberger
- Vienna Hepatic Hemodynamic Laboratory, Medical University of Vienna, Währinger Gürtel 18-20, Vienna, Austria.
- Division of Gastroenterology and Hepatology, Department of Internal Medicine III, Medical University of Vienna, Währinger Gürtel 18-20, 1090, Vienna, Austria.
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