Open Access, Peer-reviewed
pISSN 2288-3886
eISSN 2288-3959
    J Nutr Health. 2024 Jun;57(3):282-291. English.
    Published online Jun 25, 2024.
    https://doi.org/10.4163/jnh.2024.57.3.282
    © 2024 The Korean Nutrition Society
    Original Article

    Impact of dietary fiber intake on non-alcoholic fatty liver disease risk in Korean patients with obesity and type 2 diabetes mellitus

    Ji-Sook Park,1 Hina Akbar,2 Young-Seol Kim,3 and Jung-Eun Yim1,2
      • 1Department of Food and Nutrition, Changwon National University, Changwon 51140, Republic of Korea.
      • 2Interdisciplinary Program in Senior Human Ecology, Changwon National University, Changwon 51140, Republic of Korea.
      • 3Department of Endocrinology and Metabolism, Kyung Hee University School of Medicine, Seoul 02447, Republic of Korea.
    • Correspondence to Jung-Eun Yim. Department of Food and Nutrition, Changwon National University, 20 Changwondaehak-ro, Uichang-gu, Changwon 51140, Republic of Korea. Tel: +82-55-213-3517, Email: [email protected]
    Received March 27, 2024; Revised June 12, 2024; Accepted June 18, 2024.

    This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

    Abstract

    Purpose

    Korean patients with type 2 diabetes mellitus (T2DM) and obesity are at a high risk of developing severe non-alcoholic fatty liver disease (NAFLD). This study examined the dietary intakes and compared the risks of NAFLD-related complications in Korean patients with T2DM and obesity.

    Methods

    Data from the Korean National Diabetes Program cohort were used to study patients with T2DM. Two hundred and sixty-five obese patients with T2DM (body mass index ≥ 25 kg/m2) were classified into NAFLD and non-NAFLD groups. The nutrient intake was analyzed using a 24-hour dietary recall questionnaire. Anthropometric and biochemical data were also obtained. Statistical analyses were performed to determine the significant differences between the 2 groups.

    Results

    The serum gamma-glutamyl transpeptidase levels in obese patients with T2DM and NAFLD were significantly higher than in obese T2DM patients without NAFLD (p < 0.05). The serum glucose and lipid profiles showed no significant differences between the NAFLD and non-NAFLD groups. The carbohydrate, protein, and fat levels also did not differ significantly. The results showed that the fiber intake of the NAFLD and non-NAFLD groups was 14.11 ± 3.86 g/100 kcal and 15.70 ± 4.56 g/1,000 kcal, respectively, showing that the dietary fiber intake of the non-NAFLD group was significantly higher (p < 0.05). A correlation was observed between total fiber intake and γ-glutamyl transpeptidase in either patient group. In addition, the odds ratio of developing NAFLD was 0.29× lower when the fiber was consumed at 125% of adequate intake.

    Conclusions

    A higher dietary fiber intake may reduce the risk of NAFLD in obese patients with T2DM. The dietary intake of Korean obese patients with T2DM should include and be enriched in dietary fiber to aid in preventing and treating NAFLD.

    Keywords
    non-alcoholic fatty liver disease; type 2 diabetes mellitus; obesity; dietary fiber

    INTRODUCTION

    Diabetes mellitus, which has a rapidly increasing incidence and prevalence, is a serious public health concern that causes significant morbidity, disability, and mortality worldwide [1]. According to the International Diabetes Federation, 536.6 million adults worldwide had diabetes in 2021, and it is predicted that it will increase to 783.2 million by 2045 [2].

    Non-alcoholic fatty liver disease (NAFLD) is an accumulate of fat in the liver cell of individuals without excessive alcohol intake. According to statistics, the prevalence of NAFLD is estimated to be 25% worldwide [3] and has been rapidly rising over the past 10 years. Asia has a higher prevalence of NAFLD (27%) than either North America or Europe (24%) [4]. Increased industrialization in many Asian countries has altered many lifestyles to become more sedentary and has resulted in higher levels of overnutrition—both of which are significantly associated with metabolic disorders [3].

    Several studies have indicated that NAFLD is not limited to liver damage—as it is also linked to metabolic syndrome, type 2 diabetes mellitus (T2DM), cardiovascular disease [5], and chronic kidney disease [6]. The prevalence of NAFLD is higher in individuals with an elevated body mass index (BMI) and among patients with T2DM [7]. The risk factors for NAFLD and T2D are comparable, and their association has been further highlighted by their epidemiologies and pathophysiologies [5].

    T2DM can increase the risk of NAFLD and related mortality [8], such as liver cirrhosis and hepatocellular carcinoma [9]. In addition, NAFDL also induces the risk of T2DM, leads to disorders of lipid and glucose metabolism, and increases the prevalence of diabetic microvascular disease [10]. T2DM and NAFLD present with similarly poor metabolic profiles (including genetic factors, insulin resistance, dyslipidemia, obesity, lifestyle factors, and others) [11]. Animal experiments and cell-based studies have demonstrated that insulin resistance plays an essential role in the mechanism behind NAFLD pathogenesis [12].

    The impact of NAFLD on public health may be reduced by identifying controllable risk factors for its early prevention [13]. Dietary factors may be among the most important factors [14]; however, optimal diets for preventing NAFLD have not yet been established. Most previous studies have examined the effects of particular foods or nutrients on NAFLD—such as choline [15], nuts [16], and raw garlic [17]. A recent study found that a higher insoluble fiber intake (> 7.5 g/day) resulted in improvements in 3 different scales of liver fibrosis (hepatic steatosis index, fatty liver index, and NAFLD liver fat score) [18].

    According to a cross-sectional study conducted in the Netherlands, participants with high fatty liver indexes had poor dietary fiber intake [19]. Another large cross-sectional study in China reported an interconnection between total dietary fiber intake and a low prevalence of newly diagnosed NAFLD [20]. Several studies have reported that dietary patterns can be used as a prophylactic prevention strategy in Korean adults at high risk of developing NAFLD [21], whereas another study concluded that dietary factors are significantly related to NAFLD in Korean adults [22]. However, no studies have yet established the association between dietary fiber intake and NAFLD prevention in Korean patients with T2DM.

    Therefore, considering the rapid increase in the prevalence of diabetes and NAFLD in Korea, it is crucial to examine the relationship between NAFLD, diabetes, and obesity in a large cohort of Korean adults to provide evidence for their prevention and treatment. This study aimed to evaluate dietary intake according to the presence or absence of NAFLD in Korean patients with T2DM and compare their risks of developing NAFLD according to their dietary intake patterns.

    METHODS

    Study design and participants

    For this investigation, we used information from the Korean National Diabetes Program (KNDP) cohort database. The KNDP is a large-scale, prospective, multicenter cohort study that collects data from Korean individuals who have type 2 diabetes and those who are at high risk for developing the disease. Patients between the ages of 40 and 63 who had T2DM and BMIs of ≥ 25 kg/m2 were recruited. The data were collected from various university hospitals in South Korea. Baseline clinical characteristics such as sex, age, BMI, blood pressure, smoking and drinking habits, glucose levels, glycated hemoglobin (HbA1c) levels, lipid profiles, and liver function indexes (blood urea nitrogen, aspartate aminotransferase [AST], alanine aminotransferase [ALT], and gamma-glutamyltranspeptidase [γGTP]) were provided by the KNDP cohort data. In total, 265 patients with T2DM were included. The KNDP cohort comprised 2 groups: patients with T2DM, both with and without NAFLD. The experimental protocol was approved by the Ethics Committee of the Kyung Hee University Hospital (KMC IRB No. 0526-04) and conformed to the ethical principles of the Declaration of Helsinki.

    Anthropometric measurements

    Anthropometric measurements were performed with the participants wearing light clothing without shoes. Blood pressure was measured using oscilometric devices after the subjects rested for at least 5 minutes in a sitting position (Inbody BPBIO320; Biospace, Seoul, Korea). Both systolic and diastolic blood pressures were recorded. Waist circumference (WC) and hip circumference (HC) were measured in cm using soft measuring tapes. WC was measured halfway between the lower borders of the thoracic cage and iliac crest. Height and weight were measured in cm and kg, respectively. Body composition of participants was analyzed using bioelectrical impedance analysis (Inbody 720; Biospace). BMI was calculated as weight (kg) divided by height squared (m2). The percentage of body fat (PBF) was also calculated for all 265 patients of both groups.

    Biochemical measurements

    Blood samples were collected after an overnight fast of at least 10 hours and stored at −70°C for subsequent assays. Biochemical data—including total cholesterol, triglycerides, high-density lipoprotein-cholesterol, low-density lipoprotein-cholesterol, AST, and ALT levels—were measured using a Toshiba 200FR Neo analyzer (Toshiba Medical System Co., Ltd., Tokyo, Japan) via the enzymatic colorimetric method. Following the manufacturer's instructions, a Toshiba 200 FR autoanalyzer (Toshiba Medical System Co., Ltd.) and an ion-exchange high-performance liquid chromatograph (Bio-Rad Laboratories, Inc., Hercules, CA, USA) were used to measure fasting plasma glucose and HbA1c levels, respectively.

    Dietary assessment

    For dietary intake, an in-person question-and-answer session was held with patients by trained certified dieticians using a 24-hour dietary recall questionnaire. Photographs and food models were used to evaluate portion sizes. A 24-hour dietary recall questionnaire was used during an in-person question-and-answer session with patients by professional dieticians with training. Portion sizes were assessed using food models and photographs. Dietary intake was analyzed using the Computer-Aided Nutrient Analysis Program version 5.0 (CAN-Pro 5.0; The Korean Nutrition Society, Seoul, Korea), which converts food consumption records to nutrient intake. Fiber intake ratio (%) was calculated by dividing the fiber intake by the adequate intake (AI) and multiplying it by 100.

    Statistical analysis

    Relative frequencies (%) and absolute frequencies (n) were used to represent categorical variables. Standard deviations ± mean values were used to represent continuous variables. Mann-Whitney U and χ2 tests were used to conduct comparisons between the 2 groups. Spearman’s correlation test was used to estimate the correlation between fiber intake and NAFLD-associated variables. Logistic regression analysis was used to assess odds ratios (ORs) and their corresponding 95% confidence intervals (95% CIs). Statistical evaluation was performed using statistical packages in SPSS version 27.0 (IBM Corp., Armonk, NY, USA), which was used to carry out all statistical analyses and data management. Statistical significance was set at p < 0.05.

    RESULTS

    Anthropometric measurements

    The 265 patients with T2DM were categorized into 2 groups: NAFLD and non-NAFLD. A total of 55 had NAFLD, and the remaining 210 fell into the non-NAFLD group. Table 1 summarizes the anthropometric characteristics (height, weight, BMI, PBF, WC, and HC) of all of the participants. Age, sex, height, and weight differed significantly between the groups (p < 0.01), with the non-NAFLD groups being older than the NAFLD one and the NAFLD group having higher height and weight measurements. However, there was no significant difference in BMI between the 2 groups.

    Table 1
    General characteristics and anthropometric measurements in patients with T2DM with and without NAFLD

    Biochemical measurements

    Table 2 presents the serum glycemic indexes and lipid profiles of all of the patients. There were no significant differences found between them in terms of HbA1c levels, as well as glycemic and lipid profiles. By contrast, representative liver function indexes showed that serum γGTP was significantly higher in the patients with NAFLD. The NAFLD group also tended to have higher ALT and AST levels than the non-NAFLD one.

    Table 2
    Biochemical profiles of patients with T2DM with and without NAFLD

    Dietary assessment

    Table 3 shows the carbohydrate, protein, fat, and fiber intakes of the participants. There were no significant differences in terms of macronutrient intakes; however, the dietary fiber intakes of the patients with T2DM who did not have NAFLD (15.70 ± 4.56 g/1,000 kcal) were significantly higher than those of the patients with NAFLD (14.1 ± 3.86 g/1,000 kcal, p < 0.05). The fiber intake ratios of the patients without NAFLD were significantly higher than that of those with NAFLD (p = 0.001).

    Table 3
    Daily nutrient intake in patients with T2DM with and without NAFLD

    Dietary fiber and NAFLD

    Fig. 1 shows the associations between fiber intake ratio and γGTP in our patients with T2DM, with and without NAFLD. The correlation between total fiber intake and γGTP was negative in both the patients with NAFLD (r = −0.345, p = 0.025) and those without (r = −0.145, p = 0.045). With an increase in the fiber intake ratio achieving AI, the risk of developing NAFLD decreased. The association between fiber intake and NAFLD is presented in Table 4. When intakes of fiber were stratified by ratio to the AI target, those with a 125% fiber intake ratio had a 0.29× lower risk of having NAFLD (OR, 0.289; 95% CI, 0.121–0.679; p < 0.01). Patients with a fiber intake ratio of 150% of the AI had 0.08× lower OR for NAFLD (OR, 0.076; 95% CI, 0.010–0.565; p < 0.05). As the ratio of fiber intake to AI increased, the OR for NAFLD tended to decrease; however, the difference was not statistically significant.

    Fig. 1
    The correlation between fiber intake ratio and γGTP in patients with type 2 diabetes mellitus and NAFLD (A) or without NAFLD (B).
    γGTP, gamma-glutamyltranspeptidase; NAFLD, non-alcoholic fatty liver disease.

    Table 4
    Logistic regression analyses to evaluate the association between fiber intake and non-alcoholic fatty liver disease

    DISCUSSION

    Over the past 10 years, the prevalence of diabetes and NAFLD has increased in several regions, including Korea, owing to decreases in health-conscious behaviors and more Westernized lifestyles [23]. This has increased the incidence of health-related problems in several Asian countries [24]. According to a recent meta-analysis, 28.5% of Asians suffer from NAFLD [25]. In one Korean cohort study, the prevalence of NAFLD was 27%, and 47% of patients with prediabetes had NAFLD [26].

    This study aimed to compare the dietary intake patterns of patients with T2DM with and without NAFLD, as well as the relationship between the anthropometric and biochemical variables associated with NAFLD. The results indicated that dietary fiber intake may be associated with NAFLD. The group with NAFLD in our patient cohort was found to have a lower overall fiber intake. Notably, we also found that a higher fiber intake was associated with a lower risk of NAFLD in patients with T2DM.

    Previous nutritional and NAFLD-related studies have mainly focused on the negative effects of fat intake. One study revealed that a high-fat diet may lead to the rapid development of NAFLD, while others have suggested an association between NAFLD and different types of fat. However, we found that the patient group with NAFLD in our cohort had a lower fiber consumption. In a cross-sectional study of healthy Dutch adults, the participants with high fatty liver indexes were shown to have lower levels of dietary fiber consumption [19]. A similar Chinese study found a negative correlation between total dietary fiber intake and NAFLD [20]. Several other studies have also investigated the relationship between dietary fiber intake and NAFLD, with findings that are consistent with ours from this study.

    Furthermore, a recent randomized controlled trial found a correlation between fiber intake and degree of liver fibrosis. That study showed that, while consuming higher fruit fiber (≥ 8.8 g/day) significantly decreased hepatic enzymes, consuming higher insoluble fiber (≥ 7.5 g/day) improved liver fibrosis [18]. Another study found that an increased intake of soluble and insoluble fibers, from 19 to 29 g/day, improved hepatic steatosis and reduced liver enzymatic activity in patients with NAFLD, potentially by altering intestinal permeability [27].

    The average dietary fiber intake of 24.5 and 26.8 g in this study was adequate, as the recommended intake for Koreans is 20 g for women and 30 g for men [28]. However, the risk of developing NAFLD was reduced when 125% of the AI for fiber (up to 37.5 g for men and up to 25 g for women) was consumed. Notably, increasing this intake ratio to 150% further reduced the risk of developing NAFLD. These results are consistent with those of another recent cross-sectional study in China [29]. As the total daily fiber intakes of the Chinese participants in that study increased, the OR 0.20 (0.16–0.25) for the risk of developing NAFLD decreased significantly [29]. Another study from Iran demonstrated that patients with NAFLD (31.2 g) consumed less dietary fiber than healthy controls (35.3 g) and reported that reduced fiber intake may play an important role in the progression of NAFLD [30]. Studies on the association between dietary fiber intake and NAFLD have reported on the intake of soluble or insoluble dietary fibers from various sources. No associations have been observed between soluble dietary fiber and insoluble fiber intake; however, a significant association was reported with higher insoluble fiber intake [20]. Regardless of the source of dietary fiber, an increased intake appears to reduce the risk of developing NAFLD [30]. There is limited research on the recommended amount of fiber intake to reduce the risk of NAFLD; however, most studies agree that increasing fiber intake is important. Notably, the American Diabetes Association recommends that men and women with diabetes maintain a dietary fiber intake of up to 38 g and up to 25 g per day, respectively [31]. Our study recommends that patients with obesity and T2DM increase their fiber intake by 1.25–1.5 times the AI to prevent and treat complications such as NAFLD.

    Although the mechanisms underlying the relationship between dietary fiber intake and NAFLD are poorly understood, several potential mechanisms have been proposed. Specifically, the pathophysiological mechanism of NAFLD has been found to include insulin resistance, hepatic lipid metabolism, and intestinal floral changes [31, 32, 33, 34]. Dietary fiber consumption can reduce postprandial blood glucose levels and stomach emptying [31]. Furthermore, research has indicated that dietary fiber intake may promote fat excretion [32]. In addition, intestinal microbes ferment dietary fiber to create short-chain fatty acids (such as propionic acid and butyric acid) [33], which control hepatic lipid metabolism and improve insulin sensitivity [34, 35]. In other words, dietary fiber helps patients with NAFLD by promoting a lower caloric intake and stimulating healthy gut microbiota, which in turn reduces inflammation and liver injury.

    This study had several notable strengths. First, a standardized approach was established and strictly maintained by researchers with specialized training. Second, we confirmed a statistically significant negative correlation between dietary fiber intake and NAFLD using various analyses. Nevertheless, the study was also subject to certain key limitations worth noting. First, because the study cohort included individuals who visited particular health screening centers in Korea for their checks, it's possible that it wasn't completely representative of the general population and that selection bias played some role in it. Second, we could not evaluate the participant's physical activity habits, which is a significant factor in NAFLD. Third, owing to the cross-sectional design of our study, we could not establish a relationship between dietary fiber intake and the risk of NAFLD.

    SUMMARY

    The purpose of this study was to investigate the dietary fiber intake in patients with T2DM, both with and without NAFLD. Dietary intake levels of total fiber—including cereals, fruits, and vegetables—were found to be negatively associated with the risk of developing NAFLD in middle-aged Korean patients with T2DM. Middle-aged patients with T2DM and obesity should therefore be advised to increase their levels of dietary fiber intake to prevent NAFLD. To further clarify this correlation, we strongly recommend conducting larger prospective surveys.

    Notes

    Funding:This work was supported by the National Research Foundation (NRF) by the Korea government (MSIT) (No. RS2023-00242278).

    Conflict of Interest:There are no financial or other issues that might lead to conflict of interest.

    Author Contributions:

    • Conceptualization: Kim YS, Yim JE.

    • Data curation: Park JS, Akbar H.

    • Investigation: Park JS, Akbar H.

    • Methodology: Yim JE.

    • Writing - original draft: Park JS.

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    MeSH Terms
    Blood Glucose
    Carbohydrates
    Cohort Studies
    Diabetes Mellitus, Type 2*
    Dietary Fiber*
    Eating
    Humans
    Lipids
    Non-alcoholic Fatty Liver Disease*
    Obesity*
    Odds Ratio
    Peptidyl Transferases
    Program
    Proteins
    Respect
    gamma-Glutamyltransferase
    Metrics
    Share
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    Tables
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