Diabetes & Metabolism Journal

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

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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
Clinical Gastroenterology and Hepatology.2024; 22(3): 488. CrossRef
Association of NAFLD/NASH, and MAFLD/MASLD with chronic kidney disease: an updated narrative review
Amedeo Lonardo
Metabolism and Target Organ Damage.2024;[Epub] CrossRef
Targeting metabolic-associated fatty liver disease in diabetic kidney disease: A call to action
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
Associations of non-invasive indices of liver steatosis and fibrosis with progressive kidney impairment in adults with type 2 diabetes
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
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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
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Jaehyun Bae, Byung-Wan Lee
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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
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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
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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

Metabolic Risk/Epidemiology
Association between Non-Alcoholic Steatohepatitis and Left Ventricular Diastolic Dysfunction in Type 2 Diabetes Mellitus: Hokyou Lee, Gyuri Kim, Young Ju Choi, Byung Wook Huh, Byung-Wan Lee, Eun Seok Kang, Bong-Soo Cha, Eun Jig Lee, Yong-ho Lee, Kap Bum Huh; Diabetes Metab J. 2020;44(2):267-276. Published online February 28, 2019; DOI: https://doi.org/10.4093/dmj.2019.0001

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Background

Impaired diastolic heart function has been observed in persons with non-alcoholic fatty liver disease (NAFLD) and/or with type 2 diabetes mellitus (T2DM). However, it is unclear whether NAFLD fibrotic progression, i.e., non-alcoholic steatohepatitis, poses an independent risk for diastolic dysfunction in T2DM. We investigated the association between liver fibrosis and left ventricular (LV) diastolic dysfunction in T2DM.

Methods

We analyzed 606 patients with T2DM, aged ≥50 years, who had undergone liver ultrasonography and pulsed-wave Doppler echocardiography. Insulin sensitivity was measured by short insulin tolerance test. Presence of NAFLD and/or advanced liver fibrosis was determined by abdominal ultrasonography and NAFLD fibrosis score (NFS). LV diastolic dysfunction was defined according to transmitral peak early to late ventricular filling (E/A) ratio and deceleration time, using echocardiography.

Results

LV diastolic dysfunction was significantly more prevalent in the NAFLD versus non-NAFLD group (59.7% vs. 49.0%, P=0.011). When NAFLD was stratified by NFS, subjects with advanced liver fibrosis exhibited a higher prevalence of diastolic dysfunction (49.0%, 50.7%, 61.8%; none, simple steatosis, advanced fibrosis, respectively; P for trend=0.003). In multivariable logistic regression, liver fibrosis was independently associated with diastolic dysfunction (odds ratio [OR], 1.58; 95% confidence interval [CI], 1.07 to 2.34; P=0.022) after adjusting for insulin resistance and cardiometabolic risk factors. This association remained significant in patients without insulin resistance (OR, 4.32; 95% CI, 1.73 to 11.51; P=0.002).

Conclusions

Liver fibrosis was associated with LV diastolic dysfunction in patients with T2DM and may be an independent risk factor for diastolic dysfunction, especially in patients without systemic insulin resistance.

Citations

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Complications
Color Doppler Ultrasonography Is a Useful Tool for Diagnosis of Peripheral Artery Disease in Type 2 Diabetes Mellitus Patients with Ankle-Brachial Index 0.91 to 1.40: Kyu Yeon Hur, Ji Eun Jun, Young Ju Choi, Yong-ho Lee, Dae Jung Kim, Seok Won Park, Byung Wook Huh, Eun Jig Lee, Sun-Ha Jee, Kap Bum Huh, Sung Hee Choi; Diabetes Metab J. 2018;42(1):63-73. Published online February 23, 2018; DOI: https://doi.org/10.4093/dmj.2018.42.1.63

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Background

The clinical utility of ankle-brachial index (ABI) is not clear in subjects with less severe or calcified vessel. Therefore, we investigated the usefulness of color Doppler ultrasonography for diagnosing peripheral artery disease (PAD) in type 2 diabetes mellitus (T2DM) subjects.

Methods

We analyzed 324 T2DM patients who concurrently underwent ABI and carotid intima-media thickness (CIMT) measurements and color Doppler ultrasonography from 2003 to 2006. The degree of stenosis in patients with PAD was determined according to Jager's criteria, and PAD was defined as grade III (50% to 99% stenosis) or IV stenosis (100% stenosis) by color Doppler ultrasonography. Logistic regression analysis and receiver operating characteristic curve analysis were performed to evaluate the risk factors for PAD in patients with ABI 0.91 to 1.40.

Results

Among the 324 patients, 77 (23.8%) had ABI 0.91 to 1.40 but were diagnosed with PAD. Color Doppler ultrasonography demonstrated that suprapopliteal arterial stenosis, bilateral lesions, and multivessel involvement were less common in PAD patients with ABI 0.91 to 1.40 than in those with ABI ≤0.90. A multivariate logistic regression analysis demonstrated that older age, current smoking status, presence of leg symptoms, and high CIMT were significantly associated with the presence of PAD in patients with ABI 0.91 to 1.40 after adjusting for conventional risk factors. CIMT showed significant power in predicting the presence of PAD in patients with ABI 0.91 to 1.40.

Conclusion

Color Doppler ultrasonography is a useful tool for the detection of PAD in T2DM patients with ABI 0.91 to 1.40 but a high CIMT.

Citations

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Optimal Waist Circumference Cutoff Value Based on Insulin Resistance and Visceral Obesity in Koreans with Type 2 Diabetes: Jung Soo Lim, Young Ju Choi, Soo-Kyung Kim, Byoung Wook Huh, Eun Jig Lee, Kap Bum Huh; Diabetes Metab J. 2015;39(3):253-263. Published online April 24, 2015; DOI: https://doi.org/10.4093/dmj.2015.39.3.253

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Background

Visceral obesity is the most powerful contributor to the development of metabolic syndrome (MetS) and cardiovascular diseases. In light of visceral obesity, however, there is a paucity of data on the appropriate cutoff point of waist circumference (WC) in subjects with type 2 diabetes. The aim of this study was to investigate the optimal cutoff value for WC that signals insulin resistance (IR) and visceral obesity in Koreans with type 2 diabetes.

Methods

We evaluated 4,252 patients with type 2 diabetes (male 2,220, female 2,032, mean age 57.24 years) who visited our clinic between January 2003 and June 2009. WC was measured at the midpoint between the lower rib and the iliac crest, and insulin sensitivity was assessed by the rate constant of plasma glucose disappearance (Kitt %/min) using an insulin tolerance test. Visceral fat thickness was measured using ultrasonography. Statistical analysis was performed using receiver operating characteristic curve.

Results

The optimal cutoff points for WC for identifying the presence of IR and visceral obesity, as well as two or more metabolic components, were 87 cm for men and 81 cm for women. Moreover, these cutoff points had the highest predictive powers for the presence of visceral obesity. The MetS defined by new criteria correlated with the increased carotid intima-media thickness in female subjects.

Conclusion

Our results suggest that the optimal cutoff values for WC in Koreans with type 2 diabetes should be reestablished based on IR and visceral obesity.

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Associations between ApoB/ApoA-I Ratios and Metabolic Syndrome and its Components in Patients with Type 2 Diabetes.: Jung Eun Kim, Wha Young Kim, Yoon Jung Lee, Ji Eun Park, Young Ju Choi, Kap Bum Huh, Ji Yun Hwang; Korean Diabetes J. 2009;33(2):143-154. Published online April 1, 2009; DOI: https://doi.org/10.4093/kdj.2009.33.2.143

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Abstract PDF

BACKGROUND
The Apolipoprotein B/apolipoprotein A-I ratio (apoB/apoA-I) is a powerful clinical indicator of metabolic syndrome. However, few studies have searched for an association between ApoB/ApoA-I and metabolic syndrome in Korean patients with type 2 diabetes. We investigated the relation between ApoB/ApoA-I and the risk of metabolic syndrome and its components. METHODS: Subjects were 812 (424 males and 388 females) Korean patients who were being treated for type 2 diabetes at Huh's Diabetes Center in Seoul. The patients were classified into quartiles (lowest:Q1-highest:Q4) of ApoB/ApoA-I by gender. Anthropometric and hematological characteristics and dietary intake using a food frequency questionnaire were assessed. RESULTS: The prevalence of metabolic syndrome in our sample was 47.9% in males and 66.5% in females. The odds ratios (OR) for metabolic syndrome and for having its components were significantly increased from Q2 to Q4 quartiles of ApoB/ApoA-I in males (OR = 5.37; 95% CI = 2.98-9.65 and OR = 7.41; 95% CI = 4.04-13.6) and females (OR = 2.57; 95% CI = 1.28-5.15 and OR = 8.49; 95% CI = 4.28-16.8). These trends withstood adjustment for age, duration of type 2 diabetes, fasting blood glucose levels, and macronutrient intake both in males (OR = 5.24; 95% CI = 2.80-9.24 and OR = 7.98; 95% CI = 4.09-15.6) and in females (OR=4.41; 95% CI = 2.26-8.61 and OR = 8.29; 95% CI = 3.85-17.8). CONCLUSION: ApoB/ApoA-I appeared to be independently associated with risk of having metabolic syndrome and its components in Korean patients with type 2 diabetes after adjustment for putative risk factors including macronutrient intake, a particularly important lifestyle factor for patients with type 2 diabetes. A follow-up study of this population should evaluate the mechanisms underlying the relation between ApoB/ApoA-I and metabolic syndrome and its components.

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