Metabolic (Dysfunction)-Associated Fatty Liver Disease in Chinese Patients with Type 2 Diabetes from a Subcenter of the National Metabolic Management Center

Guan, Conghui; Fu, Songbo; Zhen, Donghu; Yang, Kuan; An, Jinyang; Wang, Yapei; Ma, Chengxu; Jiang, Na; Zhao, Nan; Liu, Jinjin; Yang, Fang; Tang, Xulei

doi:https://doi.org/10.1155/2022/8429847

Journal of Diabetes Research

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Abstract Introduction Materials and Methods Results Discussion Data Availability Conflicts of Interest Authors’ Contributions Acknowledgments Supplementary Materials References Copyright Related Articles

Research Article | Open Access

Volume 2022 | Article ID 8429847 | https://doi.org/10.1155/2022/8429847

Metabolic (Dysfunction)-Associated Fatty Liver Disease in Chinese Patients with Type 2 Diabetes from a Subcenter of the National Metabolic Management Center

Conghui Guan,^1,2Songbo Fu,^1,2Donghu Zhen,^1,2Kuan Yang,²Jinyang An,²Yapei Wang,²Chengxu Ma,^1,2Na Jiang,²Nan Zhao,^1,2Jinjin Liu,^1,2Fang Yang,¹and Xulei Tang^1,2

Academic Editor: Ferdinando Carlo Sasso

Received02 Sept 2021

Accepted11 Jan 2022

Published28 Jan 2022

Abstract

Background. Few studies have investigated the epidemiological metabolic (dysfunction) associated with fatty liver disease (MAFLD) in China, especially among those with type 2 diabetes. Methods. We recruited 3553 patients aged 18-75 years with type 2 diabetes who underwent abdominal ultrasound and serum biochemical analyses. Patient information including demographic and anthropometric parameters was also collected. Results. Overall, 63.2% of type 2 diabetic patients had MAFLD. Among the MAFLD patients, the proportions of lean, nonobese, and obese MAFLD were 23.1%, 75.7%, and 24.3%, respectively, and the percentage of previously undiagnosed MAFLD was 42.2%. MAFLD patients were younger, had shorter diabetic duration, and had greater BMI, aspartate aminotransferase (AST), alanine aminotransferase (ALT), fasting insulin, postprandial insulin, total cholesterol, and insulin resistance levels (HOMA-IR and TyG index). Liver fibrosis diagnostic panels revealed that the proportions of elevated AST (≥40 U/L) and ALT (≥40 U/L) were 7.3% and 18.5%, respectively. The distributions of AST-to-platelet ratio index (APRI), fibrosis-4 (FIB-4) index, and nonalcoholic fatty liver disease fibrosis score (NFS) per stage were as follows: APRI—low 55.1%, indeterminate 35.3%, and high 9.5%; FIB-4—low 48.2%, indeterminate 45.3%, and high 6.5%; and NFS—low 15.0%, indeterminate 70.0%, and high 13.0%. Conclusions. MAFLD is a very common condition and generally had greater frequency of metabolic characteristics among type 2 diabetics in China. Many MAFLD patients were in the “indeterminate” or “high” stage when APRI, FIB-4, and NFS were assessed. Assessment of MAFLD should be included in the management of type 2 diabetes.

1. Introduction

Nonalcoholic fatty liver disease (NAFLD) is classically characterized by hepatic steatosis without any other etiological agents of excess fat accumulation in the liver (e.g., excessive drinking and viral hepatitis). It has become an increasingly frequent factor of end-stage liver complications and cardiovascular disease owing to its high prevalence (25.2% in global adult population) [1] in recent decades, posing a major impact on public health and a significant economic burden [2].

Of concern, the main feature of NAFLD is recognized to be a component of metabolic syndrome, which is also seen as a coexisting disease and primary driver in clinical practice [2]. Last year, a consensus statement given out by an international expert panel proposed that metabolic (dysfunction)-associated fatty liver disease (MAFLD) be used as the accurate terminology instead of NAFLD to reflect fatty liver associated with cardiometabolic factors following a set of simple, comprehensive, and easily applicable “positive” diagnoses independent of alcohol consumption [3, 4]. The newly proposed definition for MAFLD is based on hepatic steatosis along with the existence of one of the following three criteria: clinical evidence of metabolic dysfunction, type 2 diabetes, or overweight/obesity [4]. The Asian Pacific Association for the Study of the Liver (APASL) and the Chinese Society of Hepatology subsequently accepted the consensus to use MAFLD as a descriptor for fatty liver concomitant to metabolic dysfunction [5, 6]. Among such metabolic dysfunction comorbidities, type 2 diabetes is closely correlated with MAFLD and is almost the primary risk factor [7]. Thus, consistent with the growing prevalence of type 2 diabetes worldwide, the global prevalence and hazard of MAFLD have also been increasing rapidly [8]. A meta-analysis study reported the rate of type 2 diabetes as 22.51% among NAFLD patients and 43.63% among subjects with histologically proven nonalcoholic steatohepatitis (NASH) [1]. NAFLD was reported in 55.5% of people with type 2 diabetes with a >2-fold higher prevalence than in people without diabetes [9]. MAFLD is related with liver-related complications and adverse cardiometabolic outcomes [2], which support the bidirectional relationship with type 2 diabetes.

Despite its growing prevalence and concern [4], MAFLD is not properly evaluated as a familiar chronic hepatic disease, with only a few epidemiological investigations in Asia with no national surveys from any single country including China [5, 6]. Whether the expected increase in the prevalence rate of diabetes and obesity in China [10, 11] would cause a tremendous increase in the disease burden of MAFLD is a salient question. Accordingly, we aimed to use the information obtained from the National Metabolic Management Center (MMC) in Gansu province (Northwest China), including abdominal ultrasound, demographic parameters, liver chemistry, and diabetes testing profile for subjects with type 2 diabetes, to investigate the prevalence, characteristics, risk factors, and distributions of liver fibrosis scores of MAFLD. We expected this study to provide useful information on MAFLD and increase awareness regarding MAFLD in type 2 diabetic patients.

2. Materials and Methods

2.1. Participants

The MMC was established in 2016 to impart efficient diagnosis, treatment, comprehensive diabetes management, and long-term follow-up in China [12]. The First Hospital of Lanzhou University (Gansu, China) was one of the first hospitals involved in the MMC network and provided care to more than 4830 diabetes patients in Gansu province from February 2017 to May 2021. We excluded 275 participants who refused abdominal ultrasound and those with missing important covariates (e.g., liver chemistry, blood glucose, and insulin or demographic parameters), leaving 3553 participants with type 2 diabetes to be analyzed in the present study. All participants signed the written informed consent form, and the protocol of MMC has been approved by the Institutional Review Board of Ruijin Hospital (ClinicalTrials.gov number NCT03811470). All procedures were conducted in accordance with the Declaration of Helsinki.

2.2. Demographic and Anthropometric Parameters

An advanced online and offline proprietary medical record system for the MMC [12] was conducted to integrate demographic and anthropometric information (e.g., sex, age, diseases and medication history, lifestyle and dietary habits, height, and weight). Smoking was defined as “yes” if the patients smoked daily or almost daily. Drinking was defined as “yes” if the patients drank weekly or almost weekly, overlooking alcohol consumption. The consumption of vegetables per day was divided into <200 g, 200–400 g, 400–600 g, and ≥600 g. Body mass index (BMI) was counted as weight (kg)/height (m)² and stratified as normal weight (<24.0 kg/m²), overweight (24.0-27.9 kg/m²), and obese (≥28.0 kg/m²), as per the guidelines for Chinese adults [13].

2.3. Laboratory Assays

Blood samples were obtained from participants after overnight fasting (at least 8–12 h). Postprandial blood samples were obtained 2 h after consumption of a steamed bread meal to measure postprandial glucose and postprandial insulin levels. Platelets (PLTs) were determined by flow cytometry, and aspartate aminotransferase (AST), alanine aminotransferase (ALT), albumin (ALB), plasma glucose, total cholesterol (TC), triacylglycerols (TG), HDL, and LDL were detected by an automatic biochemical analyzer in the Clinical Lab in our hospital. Serum insulin was determined by electrochemiluminescence immunoassay using immunoassay analyzers. Glycated hemoglobin (HbA_1c) levels were measured using high-performance liquid chromatography. The homeostasis model assessment for insulin resistance (HOMA-IR) was counted as , and triglyceride-glucose (TyG) was calculated as .

2.4. Definitions of Type 2 Diabetes and MAFLD

The 1999 World Health Organization diagnostic criteria were used to diagnose type 2 diabetes: , postprandial blood , or self-reported diagnosed diabetes [14]. All participants underwent abdominal ultrasound examination (Madison Ultrasound Diagnostic Instrument SO-NoaCEX 8, Samsung, Korea) conducted by a senior sonographer in the Department of Ultrasound in our hospital. The imaging diagnosis of fatty liver needs to satisfy the following ultrasound findings: high echo in the proximal diffusing point of the liver, higher echo intensity in the liver than in the kidney, and unclear intrahepatic tube structure. The diagnosis of MAFLD was based on the ultrasonically diagnosed fatty liver and the presence of type 2 diabetes [4, 5].

2.5. Liver Fibrosis Scores

For the assessment of significant liver fibrosis, AST/ALT, AST-to-platelet ratio index (APRI), fibrosis-4 (FIB-4) index, and NAFLD fibrosis score (NFS) were determined according to published formulas as diagnostic panels. AST/ALT was defined as AST(U/L)/ALT(U/L) [15]; APRI as [16]; FIB-4 as [17]; and NFS as [18]. For excluding advanced liver fibrosis, cutoff points were used as per the published studies. MAFLD patients are stratified into possessing low, intermediate, or high hazard for advanced fibrosis according to the following points: APRI (0.25 and 0.5), FIB-4 (1.30 and 2.67), and NFS (−1.455 and 0.676).

2.6. Statistical Analysis

The clinical characteristics of all subjects (Table 1) and patients with MAFLD according to BMI category (Table 2) are described. Data are shown as or median (25^th percentile, 75^th percentile) values for continuous variables and as frequency (%) for categorical variables. values were calculated using -tests, nonparametric tests, and chi-squared tests for normal distribution variables, nonnormal distribution variables, and classified variables. To identify the most important factors predicting the outcome of MAFLD in type 2 diabetes, a logistic regression model was performed (Figure 1). Confounders included sex, age, duration of diabetes, BMI, TyG index, lifestyle behaviors (smoking and drinking status), dietary habits (consumption of vegetables), and the use of antihypertensive agents, lipid-lowering agents, insulin, or noninsulin hypoglycemic agents. The results from the logistic regression model were presented as odds ratios (ORs) and 95% CIs. Statistical significance was defined as a two-sided value < 0.05. The IBM SPSS Statistics 26 software (IBM Corporation, Armonk, NY, USA) was used for all analyses.

3. Results

3.1. Clinical Characteristics

The study included 3553 subjects aged 18-75 years with type 2 diabetes. Of the total patients, 66.3% were males; the mean age of the total study population was 56.1 (SD, 10.1) years, and the mean BMI was 25.3 (SD, 3.3) kg/m². Among participants, 40.4% had a history of hypertension and 37.9% had a history of dyslipidemia. The prevalence of MAFLD was 63.2%. Among the MAFLD patients, the percentage of previously undiagnosed MAFLD was 42.2% (data not shown). Patients with MAFLD were younger, had a shorter diabetic duration and greater BMI, AST, ALT, ALB, fasting insulin, postprandial insulin, TC, TG, LDL, HOMA-IR, and TyG index levels, and included higher percentages of individuals with histories of smoking, drinking, hypertension, and dyslipidemia than non-MAFLD patients (all ) (Table 1). The same study characteristics in Table 1, stratified by BMI, in patients with MAFLD are shown in Table 2. The proportions of lean (), nonobese (), and obese () MAFLD patients were 23.1%, 75.7%, and 24.3%, respectively. Obese MAFLD patients were younger, had lower levels of postprandial glucose and shorter diabetic duration, had greater levels of AST, ALT, fasting insulin, postprandial insulin, TG, HOMA-IR index, and TyG index, and had higher percentages of individuals with hypertension and dyslipidemia histories than subjects with lean or nonobese MAFLD (all ). No significant associations were found in PLT, fasting glucose, TC, LDL, HbA_1c, and the frequency of individuals with histories of smoking and drinking among lean, nonobese, and obese MAFLD (all ) (Table 2).

3.2. Risk Factors

A binary logistic regression analysis revealed that BMI, TyG index, drinking, and lipid-lowering agents were positively related to MAFLD presence (all ), whereas male sex and diabetic duration were negatively related to MAFLD presence (all ). Notably, among type 2 diabetics, those with ≥600 g consumption of vegetables had more than a 30% reduction in MAFLD risk compared to those with <200 g consumption () (Figure 1).

3.3. Distributions of Liver Fibrosis Scores

We also analyzed the distributions and levels of noninvasive liver fibrosis diagnostic panels (including AST/ALT, APRI, Fib-4, and NFS index) in lean, nonobese, and obese MAFLD patients (Figure 2). The entire distribution of liver fibrosis diagnostic scores and the statistic difference is shown in Supplementary Table 1. A significant correlation between BMI and liver fibrosis diagnostic scores was observed. Obese MAFLD patients had higher proportions of elevated AST, ALT, APRI, and NFS scores and a greater proportion of “high risk” for advanced fibrosis for APRI and NFS ( and ).

(a)

(b)

(c)

(d)

Figure 2

(a) Proportions of patients having plasma AST or ALT in total MAFLD, lean, nonobese, and obese MAFLD. (b) Distributions of noninvasive liver fibrosis scores in MAFLD patients. (c) Proportions of patients having “intermediate” risk of fibrosis for each score in lean, nonobese, and obese MAFLD patients. (d) Proportions of patients having “high” risk of fibrosis for each score in lean, nonobese, and obese MAFLD patients. AST: aspartic acid aminotransferase; ALT: alanine aminotransferase; APRI: AST-to-platelet ratio index; FIB-4: fibrosis-4 index; NFS: nonalcoholic fatty liver disease fibrosis score.

4. Discussion

4.1. Prevalence and Awareness of MAFLD

Mainland China has seen a rapid increase in the burden of metabolic diseases owing to rapid economic transition and unhealthy lifestyles [19]. The latest prevalence of diabetes diagnosed by the American Diabetes Association criteria was 12.8% [11], and the rate of overweight/obesity exceeded 50% [10] among Chinese adults. MAFLD, earlier termed as NAFLD, was suggested as a more appropriate overarching nomenclature to emphasize the dominant driver of cardiometabolic elements in the process of fatty liver [3, 4]. This disease has affected more than one billion people worldwide [20], placing a major burden on the healthcare field and the economy.

This large single-center survey indicated that 63.2% of 18–75-year-old type 2 diabetics had MAFLD in China. This article is the first to focus on NAFLD/MAFLD in Chinese diabetes patients with a fair-sized sample volume and the first in China aimed at establishing the disease burden in type 2 diabetes patients seeking hospitalized care. Using the new MAFLD diagnostic criteria, one study from Hong Kong census database including 922 adults reported the prevalence of MAFLD as 25.9% [21]. Two studies, each including 384 and 339 patients with type 2 diabetes from Anhui province (East China), reported the prevalence of NAFLD as evaluated by ultrasonography to be 58.67% [22] and 68% [23], respectively. The 63.2% prevalence identified in our study is in line with these two studies in China and is higher than a global meta-analysis study based on ultrasound (which reported a prevalence of 55.5%) [9]. The prevalence from our study is lower than that observed by other investigators using transient elastography in European (Italy) [24] and Asian (Malaysia [25], Singapore [26], and Vietnam [27]) cohorts, as well as in the USA [28, 29], and is also lower than that using liver biopsy [30]. While MAFLD rates vary [4], the deviation between the present participants and the other Chinese studies may be ascribed to the special patients from Gansu province (an economically underdeveloped region in China) and the modest sensitivity of ultrasound in our analysis. China has released clear national plans for viral hepatitis; however, policies on fatty liver disease are less well formulated than those for other liver diseases and metabolic comorbidities, such as cardiovascular disease and diabetes. MAFLD is usually overlooked in clinical practice, especially by doctors treating diabetes, although it affects more than half of type 2 diabetics. Significant fibrosis was associated with increased risk of macrovascular and microvascular complications in type 2 diabetes; moreover, no recommendations have been included in the guidelines for the prevention and treatment of type 2 diabetes mellitus in China (2020 edition) [31] to date. In this survey, over 40% of MAFLD were previously undiagnosed patients, suggesting that the healthcare system needs further attention and more screening methods for MAFLD in the diabetes division. Type 2 diabetic Chinese patients with MAFLD were more youthful and had shorter diabetic duration than non-MAFLD patients, which encouraged us to regularly detect hepatic steatosis in newly diagnosed diabetes. Meanwhile, diet, lifestyle changes, and antidiabetic medications [32] may be beneficial for MAFLD.

4.2. Metabolic Characteristics

MAFLD is considered a metabolic hepatic disease. Recognizing the characteristics of MAFLD is instrumental in developing guidance for patient care. This survey indicated that MAFLD patients had greater BMI, lipid, and insulin resistance (e.g., high fasting and postprandial insulin, HOMA-IR, and TyG index) levels and had higher proportions of those who smoked and drank than those without MAFLD. However, the binary logistic regression suggested that age, TC, TG, LDL, smoking, and hypoglycemic agents had no relationship with the presence of MAFLD. In most metabolic studies, Asians were more likely to get insulin resistance than Caucasians [33] or European individuals [34] despite having a parallel or lower BMI. Therefore, specific BMI cutoff points have been proposed for the Asian people [35], particularly the Chinese [13]. The risk causes for MAFLD in Asians and those in Westerners are coincidental [5]. The role of dietary habits, such as the amount of vegetables consumed, has not been well assessed. Notably, in type 2 diabetics, those with ≥600 g consumption of vegetables had more than a 30% reduction in MAFLD risk than those with <200 g consumption. Although the incidence of MAFLD is notably increased accompanied by BMI, it is also being diagnosed increasingly in lean and nonobese persons. The proportions of lean (23.1%) and nonobese MAFLD (75.7%) patients in the type 2 diabetes population were higher than those of MAFLD patients in the general crowd (lean: 19.2%, nonobese: 40.8%) [36]. Unlike MAFLD versus non-MAFLD, there were no significant associations between fasting glucose, TC, LDL, HbA_1c, and the frequency of individuals who smoked and drank when comparing obese versus nonobese or lean MAFLD patients. These outcomes indicate that obesity has more effect on liver enzymes and insulin resistance than glucose and lipids for MAFLD. Thus, adopting the proposed new definition of fatty liver (MAFLD) has multiple advantages, including capturing its primary drivers, the entire spectrum of the disease, and coexisting disease modifiers in order to promote improved lifestyles on one’s own initiative and have positive public health and political outcomes. No approved drug therapy currently exists [4], and lifestyle modifications containing diet and exercise are still cornerstone intervention means [5]. Lessons can be drawn from diabetologists and cardiologists who have successfully treated diseases by correcting unhealthy lifestyle, obesity, smoking, and alcohol abuse.

4.3. Noninvasive Tests (Liver Fibrosis Scores)

The majority of MAFLD patients are stable and asymptomatic until they progress to inflammatory injury or cirrhosis [2]. One of the strongest causes in the development of MAFLD to cirrhosis or other end-stage liver disease is type 2 diabetes [4]. A meta-analyses found that fibrosis progression accelerated significantly more in NASH than in nonalcoholic fatty liver (NAFL, the early stage of MAFLD) [37] and that nearly 20% of NASH patients can be sorted into “rapid progressors” [38]. To distinguish the “rapid progressors” is an urgent issue, especially for diabetes. The International Expert Consensus Statement [4] and ASPAL [5] both recommended that ultrasound is the preferred checking method for hepatic steatosis. Noninvasive fibrosis diagnostic scores, such as APRI, FIB-4, and NFS, are commonly used to exclude advanced fibrosis because of their fine negative predictive values, in spite of the modest accuracy [5]. Although transient elastography is more precise than ultrasound and is widely used in liver disease branch [39], it is also expensive and still cannot replace liver biopsy. ASPAL suggested that transient elastography and/or fibrosis diagnostic scores are inferior to liver biopsy for confirming significant or advanced fibrosis and require further confirmation [5]. When biochemical diagnostic scores in type 2 diabetics with MAFLD were assessed in our study, the proportions of patients in the “indeterminate” and “high” zones were 44.9~85.0%. Whether they all require liver biopsy is a pertinent question. Chan et al. [40] indicated that the use of NFS or FIB-4 together with transient elastography for patients with intermediate or high scores appeared to be the optimal approach. A standardized official diagnostic method and procedure for MAFLD should be considered.

4.4. Limitations

The strength of this study is incorporating plentiful patients diagnosed with type 2 diabetes who underwent standardized abdominal ultrasonography and laboratory measurement. Our study may still have some limitations. First, this single-center design failed to investigate the comprehensive condition of MAFLD in type 2 diabetes Chinese patients. Second, for the detection of steatosis, ultrasound has limited sensitivity for light fatty liver and in individuals with a [4]. However, ultrasonography scan is still proposed as the preferred means for MAFLD [4, 5]. Finally, the hospitalized type 2 diabetic participants may limit the universality of the findings. Yet, despite these deficiencies, this research is the first to demonstrate the condition of MAFLD in Chinese patients with type 2 diabetes to a great extent. These findings may provide useful information to guide policymaking in the course of MAFLD management in type 2 diabetics.

4.5. Conclusions and Policy Implications

MAFLD is a very common condition and generally had greater frequency of metabolic characteristics among type 2 diabetics in China. Many MAFLD patients were classified in the “intermediate” or “high” stage after APRI, FIB-4, and NFS assessment. This research reminded doctor, drug companies, and administrative departments to emphasize the need for better treatment regimens and attach the assessment of MAFLD and related liver fibrosis into the management procedure of type 2 diabetes.

Data Availability

All data used to support the findings of this study are available from the corresponding author upon reasonable request.

Conflicts of Interest

The authors declare no conflicts of interest.

Authors’ Contributions

C.G. was the first author and contributed to the implementation of study, data analysis, and manuscript preparation; S.F. and D.Z. contributed to the implementation of the study; K.Y., J.A., Y.W., C.M., N.Z., J.L., N.J., and F.Y. contributed to data collection and anthropometry measurements. X.T. is the guarantor of this work and, as such, had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Acknowledgments

This study was supported by the National Key Research and Development Program of China (2018YFC1313900 and 2018YFC1313901), the fund from the First Hospital of Lanzhou University (ldyyyn2019-95), and the Special Funds of Science and Technology Development of the Chinese Central Government to Guide Local in 2020.

Supplementary Materials

Supplementary Table 1: the entire distribution of liver fibrosis diagnostic scores and the statistic difference according to different MAFLD categories. (Supplementary Materials)

References

Z. M. Younossi, A. B. Koenig, D. Abdelatif, Y. Fazel, L. Henry, and M. Wymer, “Global epidemiology of nonalcoholic fatty liver disease-meta-analytic assessment of prevalence, incidence, and outcomes,” Hepatology, vol. 64, no. 1, pp. 73–84, 2016.
View at: Google Scholar
E. E. Powell, V. W. Wong, and M. Rinella, “Non-alcoholic fatty liver disease,” The Lancet, vol. 397, no. 10290, pp. 2212–2224, 2021.
View at: Publisher Site | Google Scholar
M. Eslam, A. J. Sanyal, J. George et al., “MAFLD: a consensus-driven proposed nomenclature for metabolic associated fatty liver disease,” Gastroenterology, vol. 158, no. 7, pp. 1999–2014.e1, 2020.
View at: Publisher Site | Google Scholar
M. Eslam, P. N. Newsome, S. K. Sarin et al., “A new definition for metabolic dysfunction-associated fatty liver disease: an international expert consensus statement,” Journal of Hepatology, vol. 73, no. 1, pp. 202–209, 2020.
View at: Publisher Site | Google Scholar
M. Eslam, S. K. Sarin, V. W. Wong et al., “The Asian Pacific Association for the Study of the Liver clinical practice guidelines for the diagnosis and management of metabolic associated fatty liver disease,” Hepatology International, vol. 14, no. 6, pp. 889–919, 2020.
View at: Publisher Site | Google Scholar
“The Chinese Society of Hepatology position statement on the redefinition of fatty liver disease,” 2021, https://www.sciencedirect.com/science/article/pii/S0168827821003329.
View at: Google Scholar
S. Cernea and I. Raz, “NAFLD in type 2 diabetes mellitus: still many challenging questions,” Diabetes/Metabolism Research and Reviews, vol. 37, no. 2, article e3386, 2021.
View at: Publisher Site | Google Scholar
J. Li, B. Zou, Y. H. Yeo et al., “Prevalence, incidence, and outcome of non-alcoholic fatty liver disease in Asia, 1999-2019: a systematic review and meta-analysis,” The Lancet Gastroenterology & Hepatology, vol. 4, no. 5, pp. 389–398, 2019.
View at: Publisher Site | Google Scholar
Z. M. Younossi, P. Golabi, L. de Avila et al., “The global epidemiology of NAFLD and NASH in patients with type 2 diabetes: a systematic review and meta-analysis,” Journal of Hepatology, vol. 71, no. 4, pp. 793–801, 2019, 10.1016/j.jhep.2019.06.021.
View at: Google Scholar
“The Report on Nutrition and Chronic Diseases of Chinese Residents,” Tech. Rep., 2020, http://www.nhc.gov.cn/xcs/s3574/202012/bc4379ddf4324e7f86f05d31cc1c4982.shtml.
View at: Google Scholar
Y. Li, D. Teng, X. Shi et al., “Prevalence of diabetes recorded in mainland China using 2018 diagnostic criteria from the American Diabetes Association: national cross sectional study,” BMJ, vol. 369, article m997, 2020.
View at: Publisher Site | Google Scholar
Y. Zhang, W. Wang, and G. Ning, “Metabolic Management Center: an innovation project for the management of metabolic diseases and complications in China,” Journal of Diabetes, vol. 11, no. 1, pp. 11–13, 2019.
View at: Google Scholar
C. Chen and F. C. Lu, “The guidelines for prevention and control of overweight and obesity in Chinese adults,” Biomedical and Environmental Sciences, vol. 17, pp. 1–36, 2004.
View at: Google Scholar
M. M. Gabir, R. L. Hanson, D. Dabelea et al., “The 1997 American Diabetes Association and 1999 World Health Organization criteria for hyperglycemia in the diagnosis and prediction of diabetes,” Diabetes Care, vol. 23, no. 8, pp. 1108–1112, 2000.
View at: Publisher Site | Google Scholar
A. L. Williams and J. H. Hoofnagle, “Ratio of serum aspartate to alanine aminotransferase in chronic hepatitis relationship to cirrhosis,” Gastroenterology, vol. 95, no. 3, pp. 734–739, 1988.
View at: Publisher Site | Google Scholar
C. T. Wai, J. K. Greenson, R. J. Fontana et al., “A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C,” Hepatology, vol. 38, no. 2, pp. 518–526, 2003.
View at: Publisher Site | Google Scholar
P. Loria, G. Marchesini, F. Nascimbeni et al., “Cardiovascular risk, lipidemic phenotype and steatosis. A comparative analysis of cirrhotic and non-cirrhotic liver disease due to varying etiology,” Atherosclerosis, vol. 232, no. 1, pp. 99–109, 2014.
View at: Publisher Site | Google Scholar
P. Angulo, J. M. Hui, G. Marchesini et al., “The NAFLD fibrosis score: a noninvasive system that identifies liver fibrosis in patients with NAFLD,” Hepatology, vol. 45, no. 4, pp. 846–854, 2007.
View at: Publisher Site | Google Scholar
W. Fu, C. Wang, L. Zou et al., “Association of adiposity with diabetes: a national research among Chinese adults,” Diabetes/Metabolism Research and Reviews, vol. 37, no. 5, article e3380, 2021.
View at: Publisher Site | Google Scholar
Z. Younossi, Q. M. Anstee, M. Marietti et al., “Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention,” Nature Reviews Gastroenterology & Hepatology, vol. 15, no. 1, pp. 11–20, 2018.
View at: Publisher Site | Google Scholar
V. W. Wong, G. L. Wong, J. Woo et al., “Impact of the new definition of metabolic associated fatty liver disease on the epidemiology of the disease,” Clinical Gastroenterology and Hepatology, vol. 19, no. 10, pp. 2161–2171, 2021.
View at: Google Scholar
Q. Zhou, Y. Wang, J. Wang et al., “Prevalence and risk factor analysis for the nonalcoholic fatty liver disease in patients with type 2 diabetes mellitus,” Medicine, vol. 100, no. 10, article e24940, 2021.
View at: Publisher Site | Google Scholar
Y. Zhang, J. Li, Y. Ni, Y. Wang, and H. Liu, “Correlational study on the levels of 25-hydroxyvitamin D and non-alcoholic fatty liver disease in type 2 diabetic patients,” BMC Endocrine Disorders, vol. 21, no. 1, p. 100, 2021.
View at: Publisher Site | Google Scholar
A. Mantovani, T. Turino, M. G. Lando et al., “Screening for non-alcoholic fatty liver disease using liver stiffness measurement and its association with chronic kidney disease and cardiovascular complications in patients with type 2 diabetes,” Diabetes & Metabolism, vol. 46, no. 4, pp. 296–303, 2020.
View at: Google Scholar
L. L. Lai, W. N. I. Wan Yusoff, S. R. Vethakkan, N. R. Nik Mustapha, S. Mahadeva, and W. K. Chan, “Screening for non-alcoholic fatty liver disease in patients with type 2 diabetes mellitus using transient elastography,” Journal of Gastroenterology and Hepatology, vol. 34, no. 8, pp. 1396–1403, 2019.
View at: Publisher Site | Google Scholar
K. Chen, W. K. Sng, J. H. Quah et al., “Clinical spectrum of non-alcoholic fatty liver disease in patients with diabetes mellitus,” PLoS One, vol. 15, no. 8, article e0236977, 2020.
View at: Publisher Site | Google Scholar
T. T. K. Tuong, D. K. Tran, P. Q. T. Phu, T. N. D. Hong, T. Chu Dinh, and D. T. Chu, “Non-alcoholic fatty liver disease in patients with type 2 diabetes: evaluation of hepatic fibrosis and steatosis using Fibroscan,” Diagnostics, vol. 10, no. 3, p. 159, 2020.
View at: Publisher Site | Google Scholar
R. Kwok, K. C. Choi, G. L. Wong et al., “Screening diabetic patients for non-alcoholic fatty liver disease with controlled attenuation parameter and liver stiffness measurements: a prospective cohort study,” Gut, vol. 65, no. 8, pp. 1359–1368, 2016.
View at: Publisher Site | Google Scholar
R. Lomonaco, E. Godinez Leiva, F. Bril et al., “Advanced liver fibrosis is common in patients with type 2 diabetes followed in the outpatient setting: the need for systematic screening,” Diabetes Care, vol. 44, no. 2, pp. 399–406, 2021.
View at: Publisher Site | Google Scholar
M. Masarone, V. Rosato, A. Aglitti et al., “Liver biopsy in type 2 diabetes mellitus: steatohepatitis represents the sole feature of liver damage,” PLoS One, vol. 12, no. 6, article e0178473, 2017.
View at: Publisher Site | Google Scholar
Chinese Diabetes Society, “Guideline for the prevention and treatment of type 2 diabetes mellitus in China (2020 edition),” Chinese Journal of Diabetes Mellitus, vol. 13, pp. 315–409, 2021.
View at: Google Scholar
T. Salvatore, P. C. Pafundi, F. Morgillo et al., “Metformin: an old drug against old age and associated morbidities,” Diabetes Research and Clinical Practice, vol. 160, article 108025, 2020.
View at: Publisher Site | Google Scholar
M. Chandalia, P. Lin, T. Seenivasan et al., “Insulin resistance and body fat distribution in South Asian men compared to Caucasian men,” PLoS One, vol. 2, no. 8, article e812, 2007.
View at: Publisher Site | Google Scholar
K. F. Petersen, S. Dufour, J. Feng et al., “Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 48, pp. 18273–18277, 2006.
View at: Publisher Site | Google Scholar
WHO Expert Consultation, “Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies,” The Lancet, vol. 363, no. 9403, pp. 157–163, 2004.
View at: Publisher Site | Google Scholar
Q. Ye, B. Zou, Y. H. Yeo et al., “Global prevalence, incidence, and outcomes of non-obese or lean non-alcoholic fatty liver disease: a systematic review and meta-analysis,” The Lancet Gastroenterology & Hepatology, vol. 5, no. 8, pp. 739–752, 2020.
View at: Publisher Site | Google Scholar
S. Singh, A. M. Allen, Z. Wang, L. J. Prokop, M. H. Murad, and R. Loomba, “Fibrosis progression in nonalcoholic fatty liver vs nonalcoholic steatohepatitis: a systematic review and meta-analysis of paired-biopsy studies,” Clinical Gastroenterology and Hepatology, vol. 13, no. 4, pp. 643–654.e9, 2015.
View at: Publisher Site | Google Scholar
S. McPherson, T. Hardy, E. Henderson, A. D. Burt, C. P. Day, and Q. M. Anstee, “Evidence of NAFLD progression from steatosis to fibrosing-steatohepatitis using paired biopsies: implications for prognosis and clinical management,” Journal of Hepatology, vol. 62, no. 5, pp. 1148–1155, 2015.
View at: Publisher Site | Google Scholar
P. J. Eddowes, M. Sasso, M. Allison et al., “Accuracy of FibroScan controlled attenuation parameter and liver stiffness measurement in assessing steatosis and fibrosis in patients with nonalcoholic fatty liver disease,” Gastroenterology, vol. 156, no. 6, pp. 1717–1730, 2019.
View at: Publisher Site | Google Scholar
W. K. Chan, S. Treeprasertsuk, G. B. Goh et al., “Optimizing use of nonalcoholic fatty liver disease fibrosis score, fibrosis-4 score, and liver stiffness measurement to identify patients with advanced fibrosis,” Clinical Gastroenterology and Hepatology, vol. 17, no. 12, pp. 2570–2580.e37, 2019.
View at: Publisher Site | Google Scholar

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Copyright © 2022 Conghui Guan et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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