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Original Article
Complications
Non-Alcoholic Fatty Liver Disease with Sarcopenia and Carotid Plaque Progression Risk in Patients with Type 2 Diabetes Mellitus
Yongin Cho, Hye-Sun Park, Byung Wook Huh, Yong-ho Lee, Seong Ha Seo, Da Hea Seo, Seong Hee Ahn, Seongbin Hong, So Hun Kim
Diabetes Metab J. 2023;47(2):232-241.   Published online January 19, 2023
DOI: https://doi.org/10.4093/dmj.2021.0355
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  • 4 Crossref
AbstractAbstract PDFSupplementary MaterialPubReader   ePub   
Background
We aimed to evaluate whether non-alcoholic fatty liver disease (NAFLD) with or without sarcopenia is associated with progression of carotid atherosclerosis in patients with type 2 diabetes mellitus (T2DM).
Methods
We investigated 852 T2DM patients who underwent abdominal ultrasonography, bioelectrical impedance analysis, and carotid artery ultrasonography at baseline and repeated carotid ultrasonography after 6 to 8 years. NAFLD was confirmed by abdominal ultrasonography, and sarcopenia was defined as a sex-specific skeletal muscle mass index (SMI) value <2 standard deviations below the mean for healthy young adults. SMI was calculated by dividing the sum of appendicular skeletal mass by body weight. We investigated the association between NAFLD with or without sarcopenia and the progression of carotid atherosclerosis.
Results
Of the 852 patients, 333 (39.1%) were classified as NAFLD without sarcopenia, 66 (7.7%) were classified as sarcopenia without NAFLD, and 123 (14.4%) had NAFLD with sarcopenia at baseline. After 6 to 8 years, patients with both NAFLD and sarcopenia had a higher risk of atherosclerosis progression (adjusted odds ratio, 2.20; P<0.009) than controls without NAFLD and sarcopenia. When a subgroup analysis was performed on only patients with NAFLD, female sex, absence of central obesity, and non-obesity were significant factors related to increased risk of plaque progression risk in sarcopenic patients.
Conclusion
NAFLD with sarcopenia was significantly associated with the progression of carotid atherosclerosis in T2DM patients.

Citations

Citations to this article as recorded by  
  • Metabolic-associated fatty liver disease and sarcopenia: A double whammy
    Aditya Viswanath, Sherouk Fouda, Cornelius James Fernandez, Joseph M Pappachan
    World Journal of Hepatology.2024; 16(2): 152.     CrossRef
  • Prevalence and outcome of sarcopenia in non-alcoholic fatty liver disease
    Suprabhat Giri, Prajna Anirvan, Sumaswi Angadi, Ankita Singh, Anurag Lavekar
    World Journal of Gastrointestinal Pathophysiology.2024;[Epub]     CrossRef
  • Association of nonalcoholic fatty liver disease and carotid media‐intima thickness: A systematic review and a meta‐analysis
    Manouchehr Khoshbaten, Sepideh H. Maleki, Sara Hadad, Amrit Baral, Ana V. Rocha, Laxmi Poudel, Alireza Abdshah
    Health Science Reports.2023;[Epub]     CrossRef
  • Cardiometabolic risk factors in patients with type 2 diabetes and sarcopenia
    Yu. G. Samoilova, M. V. Matveeva, E. A. Khoroshunova, D. V. Podchinenova, L. L. Maksimova, G. G. Gorbach, A. B. Trivozhenko, V. A. Avkhimenko
    Cardiovascular Therapy and Prevention.2023; 23(1): 3655.     CrossRef
Response
Advanced Liver Fibrosis Is Associated with Chronic Kidney Disease in Patients with Type 2 Diabetes Mellitus and Nonalcoholic Fatty Liver Disease (Diabetes Metab J 2022;46:630-9)
Da Hea Seo, So Hun Kim
Diabetes Metab J. 2022;46(6):956-957.   Published online November 24, 2022
DOI: https://doi.org/10.4093/dmj.2022.0381
[Original]
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Original Articles
Complications
Advanced Liver Fibrosis Is Associated with Chronic Kidney Disease in Patients with Type 2 Diabetes Mellitus and Nonalcoholic Fatty Liver Disease
Da Hea Seo, Young Ju Suh, Yongin Cho, Seong Hee Ahn, Seongha Seo, Seongbin Hong, Yong-ho Lee, Young Ju Choi, Eunjig Lee, So Hun Kim
Diabetes Metab J. 2022;46(4):630-639.   Published online January 26, 2022
DOI: https://doi.org/10.4093/dmj.2021.0130
  • 5,537 View
  • 274 Download
  • 14 Web of Science
  • 16 Crossref
AbstractAbstract PDFSupplementary MaterialPubReader   ePub   
Background
Nonalcoholic fatty liver disease (NAFLD) is associated with chronic kidney disease (CKD). However, the causal relationship between NAFLD and CKD is uncertain, particularly in patients with type 2 diabetes mellitus (T2DM). We aimed to investigate the association between the presence and severity of NAFLD and incident CKD in patients with T2DM.
Methods
In this longitudinal cohort study of patients with T2DM, 3,188 patients with preserved renal function were followed up for the occurrence of incident CKD. NAFLD was defined as the presence of hepatic steatosis on ultrasonography, without any other causes of chronic liver disease. Advanced liver fibrosis of NAFLD was defined as a fibrosis-4 index ≥2.67. CKD was defined as an estimated glomerular filtration rate <60 mL/min/1.73 m2.
Results
At baseline, 1,729 (54.2%) patients had NAFLD, of whom 94 (5.4%) had advanced liver fibrosis. During the follow-up of 8.3±3.6 years, 472 (14.8%) patients developed incident CKD: 220 (15.1%) in the non-NAFLD group, 231 (14.1%) in the NAFLD without advanced fibrosis group and 28 (31.1%) in the NAFLD with advanced fibrosis group. There was no increased risk of incident CKD in the NAFLD group compared to the non-NAFLD group (P=0.435). However, among patients with NAFLD, advanced liver fibrosis was associated with an increased risk of CKD (adjusted hazard ratio, 1.75; 95% confidence interval, 1.15 to 2.66; P=0.009).
Conclusion
Advanced liver fibrosis in patients with NAFLD is independently associated with an increased risk of incident CKD in patients with T2DM.

Citations

Citations to this article as recorded by  
  • Esteatosis hepática metabólica y nefropatía diabética: una llamada a la acción
    Salvador Benlloch, Francesc Moncho, Jose Luis Górriz
    Nefrología.2024; 44(2): 129.     CrossRef
  • Longitudinal Outcomes Associated With Metabolic Dysfunction-Associated Steatotic Liver Disease: A Meta-analysis of 129 Studies
    Kai En Chan, Elden Yen Hng Ong, Charlotte Hui Chung, Christen En Ya Ong, Benjamin Koh, Darren Jun Hao Tan, Wen Hui Lim, Jie Ning Yong, Jieling Xiao, Zhen Yu Wong, Nicholas Syn, Apichat Kaewdech, Margaret Teng, Jiong-Wei Wang, Nicholas Chew, Dan Yock Young
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    Amedeo Lonardo
    Metabolism and Target Organ Damage.2024;[Epub]     CrossRef
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    Salvador Benlloch, Francesc Moncho, Jose Luis Górriz
    Nefrología (English Edition).2024;[Epub]     CrossRef
  • MAFLD and NAFLD in the prediction of incident chronic kidney disease
    So Yoon Kwon, Jiyun Park, So Hee Park, You-Bin Lee, Gyuri Kim, Kyu Yeon Hur, Janghyun Koh, Jae Hwan Jee, Jae Hyeon Kim, Mira Kang, Sang-Man Jin
    Scientific Reports.2023;[Epub]     CrossRef
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    Mei Chung Moh, Sharon Li Ting Pek, Kenny Ching Pan Sze, Serena Low, Tavintharan Subramaniam, Keven Ang, Wern Ee Tang, Simon Biing Ming Lee, Chee Fang Sum, Su Chi Lim
    Acta Diabetologica.2023; 60(6): 827.     CrossRef
  • Pancreatic beta-cell specific BAG3 knockout results in chronic hyperinsulinemia inducing insulin resistance
    Verena Damiani, Alessia Lamolinara, Ilaria Cicalini, Maria Concetta Cufaro, Francesco Del Pizzo, Federica Di Marco, Piero Del Boccio, Beatrice Dufrusine, Michael Hahne, Rossano Lattanzio, Damiana Pieragostino, Manuela Iezzi, Massimo Federici, Maria Cateri
    Molecular Metabolism.2023; 74: 101752.     CrossRef
  • Utility of non-invasive liver fibrosis markers to predict the incidence of chronic kidney disease (CKD): A systematic review, meta-analysis, and meta-regression
    Rudi Supriyadi, Theo Audi Yanto, Timotius Ivan Hariyanto, Ketut Suastika
    Diabetes & Metabolic Syndrome: Clinical Research & Reviews.2023; 17(8): 102814.     CrossRef
  • Significance of Diabetic Kidney Disease Biomarkers in Predicting Metabolic-Associated Fatty Liver Disease
    Jaehyun Bae, Byung-Wan Lee
    Biomedicines.2023; 11(7): 1928.     CrossRef
  • Hepatic Fibrosis Evaluated in Patients with Type 2 Diabetes with and without Chronic Kidney Disease
    Therese Adrian, Mads Hornum, Filip Krag Knop, Karl Bang Christensen, Thomas Almdal, Peter Rossing, Lisa Í Lídaa, Niels Søndergaard Heinrich, Vincent Oltman Boer, Anouk Marsman, Esben Thade Petersen, Hartwig Roman Siebner, Bo Feldt-Rasmussen
    Nephron.2023; 147(11): 673.     CrossRef
  • Clinical Interest of Serum Alpha-2 Macroglobulin, Apolipoprotein A1, and Haptoglobin in Patients with Non-Alcoholic Fatty Liver Disease, with and without Type 2 Diabetes, before or during COVID-19
    Olivier Deckmyn, Thierry Poynard, Pierre Bedossa, Valérie Paradis, Valentina Peta, Raluca Pais, Vlad Ratziu, Dominique Thabut, Angelique Brzustowski, Jean-François Gautier, Patrice Cacoub, Dominique Valla
    Biomedicines.2022; 10(3): 699.     CrossRef
  • Fibrosis Risk in Nonalcoholic Fatty Liver Disease Is Related to Chronic Kidney Disease in Older Type 2 Diabetes Patients
    Yifan Sun, Liang Hong, Zhe Huang, Lihong Wang, Yanqin Xiong, Shuhang Zong, Rui Zhang, Jun Liu, Shufei Zang
    The Journal of Clinical Endocrinology & Metabolism.2022; 107(9): e3661.     CrossRef
  • Beyond Liver Disease: Non-Alcoholic Fatty Liver Disease and Advanced Liver Fibrosis in Kidney Disease
    Eugene Han
    Diabetes & Metabolism Journal.2022; 46(4): 564.     CrossRef
  • A higher FIB‐4 index is associated with an increased incidence of renal failure in the general population
    Eva Maria Schleicher, Simon Johannes Gairing, Peter Robert Galle, Julia Weinmann‐Menke, Jörn M. Schattenberg, Karel Kostev, Christian Labenz
    Hepatology Communications.2022; 6(12): 3505.     CrossRef
  • Advanced Liver Fibrosis Is Associated with Chronic Kidney Disease in Patients with Type 2 Diabetes Mellitus and Nonalcoholic Fatty Liver Disease (Diabetes Metab J 2022;46:630-9)
    Ji Hye Huh
    Diabetes & Metabolism Journal.2022; 46(6): 953.     CrossRef
  • Advanced Liver Fibrosis Is Associated with Chronic Kidney Disease in Patients with Type 2 Diabetes Mellitus and Nonalcoholic Fatty Liver Disease (Diabetes Metab J 2022;46:630-9)
    Da Hea Seo, So Hun Kim
    Diabetes & Metabolism Journal.2022; 46(6): 956.     CrossRef
Complications
Serum Levels of Adipocyte Fatty Acid-Binding Protein Are Associated with Rapid Renal Function Decline in Patients with Type 2 Diabetes Mellitus and Preserved Renal Function
Da Hea Seo, Moonsuk Nam, Mihye Jung, Young Ju Suh, Seong Hee Ahn, Seongbin Hong, So Hun Kim
Diabetes Metab J. 2020;44(6):875-886.   Published online July 10, 2020
DOI: https://doi.org/10.4093/dmj.2019.0221
  • 5,630 View
  • 123 Download
  • 10 Web of Science
  • 9 Crossref
AbstractAbstract PDFPubReader   ePub   
Background

Recent studies have demonstrated that the levels of adipocyte fatty acid-binding protein (A-FABP) are closely associated with diabetic kidney disease (DKD) in patients with type 2 diabetes mellitus (T2DM). This study aimed to examine the association between serum A-FABP level and rapid renal function decline in patients with T2DM and preserved renal function.

Methods

This was a prospective observational study of 452 patients with T2DM and preserved renal function who had serial measurements of estimated glomerular filtration rate (eGFR). Rapid renal function decline was defined as an eGFR decline of >4% per year. The association between baseline serum A-FABP level and rapid renal function decline was investigated.

Results

Over a median follow-up of 7 years, 82 participants (18.1%) experienced rapid renal function decline. Median A-FABP levels were significantly higher in patients with rapid renal function decline, compared to non-decliners (20.2 ng/mL vs. 17.2 ng/mL, P=0.005). A higher baseline level of A-FABP was associated with a greater risk of developing rapid renal function decline, independent of age, sex, duration of diabetes, body mass index, systolic blood pressure, history of cardiovascular disease, baseline eGFR, urine albumin creatinine ratio, total cholesterol, glycosylated hemoglobin, high-sensitivity C-reactive protein and use of thiazolidinedione, insulin, angiotensin-converting-enzyme inhibitors and angiotensin II-receptor blockers and statin (odds ratio, 3.10; 95% confidence interval, 1.53 to 6.29; P=0.002).

Conclusion

A high level of serum A-FABP is associated with an increased risk of rapid renal function decline in patients with T2DM and preserved renal function. This suggests that A-FABP could play a role in the progression of DKD in the early stages.

Citations

Citations to this article as recorded by  
  • Serum fatty acid-binding protein 4 as a biomarker for early detection of diabetic nephropathy in type 2 diabetes
    Amr M. Shaker, Maggie E. Mohamed, Tarek Ramzy, Mayssa I. Ali
    The Egyptian Journal of Internal Medicine.2023;[Epub]     CrossRef
  • Circulating thrombospondin-2 level for identifying individuals with rapidly declining kidney function trajectory in type 2 diabetes: a prospective study of the Hong Kong West Diabetes Registry
    Chi-Ho Lee, David Tak-Wai Lui, Chloe Yu-Yan Cheung, Carol Ho-Yi Fong, Michele Mae-Ann Yuen, Wing-Sun Chow, Aimin Xu, Karen Siu-Ling Lam
    Nephrology Dialysis Transplantation.2023;[Epub]     CrossRef
  • Analysis of inflammatory cytokines and estimated glomerular filtration rate decline in Japanese patients with diabetic kidney disease: a pilot study
    Yuka Sugawara, Yosuke Hirakawa, Koki Mise, Kosuke Kashiwabara, Ko Hanai, Satoshi Yamaguchi, Akihiro Katayama, Yasuhiro Onishi, Yui Yoshida, Naoki Kashihara, Yutaka Matsuyama, Tetsuya Babazono, Masaomi Nangaku, Jun Wada
    Biomarkers in Medicine.2022; 16(10): 759.     CrossRef
  • The role of statins in patients with early diabetic nephropathy
    Xi Zhao, Shu Chun Zhou, Xiu Fang Wang, Hong Wu Liao
    Medicine.2022; 101(24): e29099.     CrossRef
  • Serum Adipocyte Fatty-Acid Binding Protein as an Independent Marker of Peripheral Artery Disease in Patients with Type-2 Diabetes Mellitus
    Bang-Gee Hsu, Chin-Yee Mah, Du-An Wu, Ming-Chun Chen
    International Journal of Environmental Research and Public Health.2022; 19(15): 9459.     CrossRef
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    Weijing Lai, Min Shi, Rongshuang Huang, Ping Fu, Liang Ma
    European Journal of Pharmacology.2022; 931: 175224.     CrossRef
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    Hong Wang, Jie Cao, Jian-bin Su, Xue-qin Wang, Xing Wang, Dong-mei Zhang, Xiao-hua Wang
    Diabetology & Metabolic Syndrome.2021;[Epub]     CrossRef
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    Emma H. Dahlström, Jani Saksi, Carol Forsblom, Nicoline Uglebjerg, Nina Mars, Lena M. Thorn, Valma Harjutsalo, Peter Rossing, Tarunveer S. Ahluwalia, Perttu J. Lindsberg, Niina Sandholm, Per-Henrik Groop
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Response
Response: Presence of Carotid Plaque Is Associated with Rapid Renal Function Decline in Patients with Type 2 Diabetes Mellitus and Normal Renal Function (Diabetes Metab J 2019;43:840–53)
Da Hea Seo, So Hun Kim, Moonsuk Nam
Diabetes Metab J. 2020;44(1):205-206.   Published online February 21, 2020
DOI: https://doi.org/10.4093/dmj.2020.0025
[Original]
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  • 1 Crossref
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Citations

Citations to this article as recorded by  
  • Mitochondrial DNA and Inflammation Are Associated with Cerebral Vessel Remodeling and Early Diabetic Kidney Disease in Patients with Type 2 Diabetes Mellitus
    Ligia Petrica, Florica Gadalean, Danina Mirela Muntean, Dragos Catalin Jianu, Daliborca Vlad, Victor Dumitrascu, Flaviu Bob, Oana Milas, Anca Suteanu-Simulescu, Mihaela Glavan, Sorin Ursoniu, Lavinia Balint, Maria Mogos-Stefan, Silvia Ienciu, Octavian Mar
    Biomolecules.2024; 14(4): 499.     CrossRef
Original Article
Complications
Presence of Carotid Plaque Is Associated with Rapid Renal Function Decline in Patients with Type 2 Diabetes Mellitus and Normal Renal Function
Da Hea Seo, So Hun Kim, Joon Ho Song, Seongbin Hong, Young Ju Suh, Seong Hee Ahn, Jeong-Taek Woo, Sei Hyun Baik, Yongsoo Park, Kwan Woo Lee, Young Seol Kim, Moonsuk Nam
Diabetes Metab J. 2019;43(6):840-853.   Published online March 12, 2019
DOI: https://doi.org/10.4093/dmj.2018.0186
  • 5,530 View
  • 57 Download
  • 17 Web of Science
  • 16 Crossref
AbstractAbstract PDFSupplementary MaterialPubReader   
Background

Recent evidences indicate that early rapid renal function decline is closely associated with the development and progression of diabetic kidney disease. We have investigated the association between carotid atherosclerosis and rapid renal function decline in patients with type 2 diabetes mellitus and preserved renal function.

Methods

In a prospective, multicenter cohort, a total of 967 patients with type 2 diabetes mellitus and preserved renal function were followed for 6 years with serial estimated glomerular filtration rate (eGFR) measurements. Common carotid intima-media thickness (CIMT) and presence of carotid plaque were assessed at baseline. Rapid renal function decline was defined as an eGFR decline >3.3% per year.

Results

Over a median follow-up of 6 years, 158 participants (16.3%) developed rapid renal function decline. While there was no difference in CIMT, the presence of carotid plaque in rapid decliners was significantly higher than in non-decliners (23.2% vs. 12.2%, P<0.001). In multivariable logistic regression analysis, presence of carotid plaque was an independent predictor of rapid renal function decline (odds ratio, 2.33; 95% confidence interval, 1.48 to 3.68; P<0.0001) after adjustment for established risk factors. The model including the carotid plaque had better performance for discrimination of rapid renal function decline than the model without carotid plaque (area under the receiver operating characteristic curve 0.772 vs. 0.744, P=0.016).

Conclusion

Close monitoring of renal function and early intensive management may be beneficial in patients with type 2 diabetes mellitus and carotid plaques.

Citations

Citations to this article as recorded by  
  • Impact of diabetes distress on glycemic control and diabetic complications in type 2 diabetes mellitus
    Hye-Sun Park, Yongin Cho, Da Hea Seo, Seong Hee Ahn, Seongbin Hong, Young Ju Suh, Suk Chon, Jeong-Taek Woo, Sei Hyun Baik, Kwan Woo Lee, So Hun Kim
    Scientific Reports.2024;[Epub]     CrossRef
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    Huijun Wen, Hai Yu
    Vascular.2023; 31(1): 90.     CrossRef
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    Yiwen Li, Yanfei Liu, Shiwei Liu, Mengqi Gao, Wenting Wang, Keji Chen, Luqi Huang, Yue Liu
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    Miriam Goepfert, Till Ittermann, Marcus Dörr, Nele Friedrich, Henry Völzke, Thomas Dabers, Stephan B Felix, Ulf Schminke, Sylvia Stracke, Sabrina von Rheinbaben
    Nephrology Dialysis Transplantation.2023; 38(11): 2598.     CrossRef
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    Luca Truscello, Dina Nobre, Vehashini Sabaratnam, Olivier Bonny, Grégoire Wuerzner, Michel Burnier, Fadi Fakhouri, Menno Pruijm, Anne Zanchi
    Frontiers in Cardiovascular Medicine.2023;[Epub]     CrossRef
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    Fatma Hilal Yagin, Seyma Yasar, Yasin Gormez, Burak Yagin, Abdulvahap Pinar, Abedalrhman Alkhateeb, Luca Paolo Ardigò
    Metabolites.2023; 13(12): 1204.     CrossRef
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    Christodoula Kourtidou, Vasileios Rafailidis, Garyfallia Varouktsi, Efthimios Kanakis, Vassilios Liakopoulos, Timoleon-Achilleas Vyzantiadis, Maria Stangou, Smaragdi Marinaki, Konstantinos Tziomalos
    Journal of Personalized Medicine.2022; 12(7): 1139.     CrossRef
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    Călin Pop, Oana Florentina Gheorghe Fronea, Ioana Antonia Branea, Lucian Mihai Itu, Roxana Darabont, Irinel Parepa, Theodora Benedek, Maria Dorobantu
    Diagnostics.2022; 12(12): 3199.     CrossRef
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    Qi Dai, Nan Chen, Ling Zeng, Xin-Jie Lin, Feng-Xiu Jiang, Xiong-Jie Zhuang, Ze-Yuan Lu
    BMC Endocrine Disorders.2021;[Epub]     CrossRef
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    Hongwei Li, Xiaolin Xu, Baoming Luo, Yuling Zhang
    Frontiers in Cardiovascular Medicine.2021;[Epub]     CrossRef
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    Le Deng, Wenjie Li, Gaosi Xu
    European Journal of Medical Research.2021;[Epub]     CrossRef
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    Rui Zhang, Yufeng Li, Xianghai Zhou, Fang Zhang, Meng Li, Simin Zhang, Xiuying Zhang, Xin Wen, Linong Ji
    Medicine.2021; 100(50): e28238.     CrossRef
  • Letter: Presence of Carotid Plaque Is Associated with Rapid Renal Function Decline in Patients with Type 2 Diabetes Mellitus and Normal Renal Function (Diabetes Metab J 2019;43:840–53)
    Min-Ji Kim, Jae-Han Jeon
    Diabetes & Metabolism Journal.2020; 44(1): 201.     CrossRef
  • Response: Presence of Carotid Plaque Is Associated with Rapid Renal Function Decline in Patients with Type 2 Diabetes Mellitus and Normal Renal Function (Diabetes Metab J 2019;43:840–53)
    Da Hea Seo, So Hun Kim, Moonsuk Nam
    Diabetes & Metabolism Journal.2020; 44(1): 205.     CrossRef
  • Serum Levels of Adipocyte Fatty Acid-Binding Protein Are Associated with Rapid Renal Function Decline in Patients with Type 2 Diabetes Mellitus and Preserved Renal Function
    Da Hea Seo, Moonsuk Nam, Mihye Jung, Young Ju Suh, Seong Hee Ahn, Seongbin Hong, So Hun Kim
    Diabetes & Metabolism Journal.2020; 44(6): 875.     CrossRef
  • Proteinuria Is Associated with Carotid Artery Atherosclerosis in Non-Albuminuric Type 2 Diabetes: A Cross-Sectional Study
    Jaehyun Bae, Yong-ho Lee, Eun Seok Kang, Bong-Soo Cha, Byung-Wan Lee
    Journal of Clinical Medicine.2020; 9(1): 136.     CrossRef

Diabetes Metab J : Diabetes & Metabolism Journal