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Original research
Fruit and vegetable consumption and non-alcoholic fatty liver disease among Korean adults: a prospective cohort study
  1. Seong-Ah Kim1,
  2. Sangah Shin1
  1. Department of Food and Nutrition, Chung-Ang University - Anseong Campus, Anseong, Korea (the Republic of)
  1. Correspondence to Sangah Shin, Department of Food and Nutrition, Chung-Ang University, 4726, Seodong-daero, Daedeokmyeon, Anseong-si, Gyeonggi-do 17546, Korea; ivory8320{at}cau.ac.kr

Abstract

Background Diet is an important risk factor contributing to the development of non-alcoholic fatty liver disease (NAFLD) and associated metabolic co-morbidities (obesity or metabolic syndrome). This study aimed to investigate the association between fruit and vegetable consumption and NAFLD risk according to sex among Korean adults.

Methods We included 52 280 participants from the Health Examinees study cohort. The cumulative average intake of fruits and vegetables was estimated using a validated semi-quantitative food frequency questionnaire. Cox proportional hazards regression analysis was performed to estimate relative risk (RR) and 95% CI of NAFLD according to the quintiles of fruit and vegetable consumption.

Results During 4.2 years of follow-up, 2130 cases of NAFLD were documented. In women, higher consumption of fruits (RR 0.77; 95% CI 0.62 to 0.96) and vegetables (RR 0.71; 95% CI 0.56 to 0.88) was associated with lower NAFLD risk (p for trend=0.0106 and 0.0071, respectively). Men showed a decreasing tendency of NAFLD risk according to vegetable consumption (p for trend =0.0374). Higher total intakes of fruits and vegetables were significantly associated with lower NAFLD risk in men (RR 0.75; 95% CI 0.62 to 0.92, p for trend =0.0047) and women (RR 0.74; 95% CI 0.59 to 0.93, p for trend =0.0021).

Conclusion Fruit intake, vegetable intake, and total fruit and vegetable intake were associated with reduced NAFLD risk. Fruit and vegetable consumption can protect against NAFLD and associated metabolic co-morbidities.

  • Cohort studies
  • epidemiology
  • epidemiology of chronic diseases
  • diet

https://doi.org/10.1136/jech-2020-214568

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    INTRODUCTION

    Non-alcoholic fatty liver disease (NAFLD) includes a wide clinical spectrum, ranging from simple steatosis to non-alcoholic steatohepatitis to eventually cirrhosis.1 Accumulating evidence indicates that NAFLD has strong associations with obesity and metabolic syndrome (MetS).1 2 Furthermore, NAFLD has been reported as an independent risk factor for various chronic diseases, most notably cardiovascular disease (CVD) and type 2 diabetes.3 4 Moreover, these metabolic co-morbidities may result from similar underlying pathophysiological pathways associated with insulin resistance, chronic systemic inflammation and dyslipidaemia.4

    Approximately 20–30% of the general population in Western countries has NAFLD,5 and its prevalence in Korea is about 19–27% among adults.6 7 Moreover, given the increasing prevalence of obesity and MetS in Korea8 as well as worldwide,9 10 there are growing concerns that health problems related to NAFLD may worsen.

    To date, several non-invasive, simple and accurate diagnostic methods for NAFLD have been used in epidemiological studies.11–13 Among the available diagnostic methods, the fatty liver index (FLI), an algorithm based on waist circumference, body mass index (BMI), and levels of triglyceride and γ-glutamyltransferase (γ-GT), has been validated against ultrasonography and applied to various populations.11 14 15

    Diet is one of the most important risk factors contributing to the development, progression and treatment of NAFLD and associated metabolic co-morbidities.16 17 A hypercaloric diet, saturated and unsaturated fatty acid intakes, and fructose intake have been known to increase the risk of NAFLD,16–19 whereas reducing caloric intake and increasing the intakes of choline, soy protein, carotenoids and dietary anthocyanins can decrease the risk of NAFLD.16 17 20 21

    With regard to fruits and vegetables, a recent nested case–control study reported that there was a significant inverse trend with increasing fruit intake and NAFLD, and vegetable consumption was not associated with NAFLD.22 Because fruits and vegetables contain large amounts of vitamins, minerals and antioxidants such as carotenoids and anthocyanins, their intake is known to be protective against many chronic diseases such as CVD, cancer and moratality,23 but they are also a major source of fructose, which can increase the risk of NAFLD.18 19 Therefore, it is necessary to examine the overall effect of fruit and vegetable consumption on the risk of NAFLD. Moreover, there is a lack of scientific evidence regarding the association between fruit and vegetable consumption and the risk of NAFLD. Ultimately, there is a need to produce evidence to establish dietary guidelines for the prevention of NAFLD. To this end, this study aimed to investigate the association between fruit and vegetable consumption and NAFLD risk according to sex among Korean adults included in the Health Examinees (HEXA) study cohort during 4.2 years of follow-up.

    METHODS

    Study population

    The HEXA study24 was a large-scale community-based prospective cohort study conducted in Korea. The baseline survey of the HEXA study was conducted from 2004 to 2013. In total, 173 357 participants aged 40–79 years were recruited from 38 general hospitals and health examination centres in eight regions of Korea. Overall, 65 642 participants of the HEXA study completed the initial follow-up survey between 2012 and 2016. Among these, those with insufficient information for the diagnosis of NAFLD based on the FLI (insufficient data on the levels of blood triglycerides and γ-GT, waist circumference, and BMI at baseline (n=5273) and follow-up (n=228)) and those diagnosed with NAFLD at baseline (n=5602) were excluded. Furthermore, we excluded participants with implausible energy intake levels (<800 or ≥4000 kcal/day in men and <500 or ≥3500 kcal/day in women) (n=2259).25 Finally, 52 280 participants (15 588 men and 36 692 women) were included in this study. The present study was conducted according to the guidelines laid down in the Declaration of Helsinki. The HEXA study was approved by the Ethics Committee of the Korean Health and the institutional review boards of all participating hospitals (IRB No. E-1503-103-657). All participants provided written informed consent prior to participating in the study.

    Diet assessment

    We used a validated semi-quantitative food frequency questionnaire (FFQ) at baseline and follow-up surveys to estimate the participants’ fruit and vegetable consumption. Regarding validity, the deattenuated, age, sex and energy intake‐adjusted correlation coefficients between the FFQ and the 12‐day diet records ranged between 0.23 (vitamin A) and 0.64 (carbohydrate) (median for all nutrients =0.39).26 Vitamin C and carotene, which are closely related to fruits and vegetables, had correlation coefficients of 0.34 and 0.31, respectively.26 The participants were asked how often they had consumed each food item on average during the past year. Among 106 food items listed in the FFQ, the following fruits were included: strawberry, muskmelon and/or melon, watermelon, peach and/or plum, banana, persimmon, tangerine, pear and/or pear juice, apple and/or apple juice, orange and/or orange juice, and grape and/or grape juice. Vegetables include radish and/or salted radish, Korean cabbages and/or Korean cabbage soup, spinach, lettuce, perilla leaf, vegetable wrap and/or vegetable salad, other green vegetables, deoduck and/or doraji (kinds of white root), bean sprouts, bracken and/or sweet potato stalk and/or stem of taro, oyster mushroom, other mushrooms, pepper leaves and/or chamnamul and/or Aster scaber, crown daisy and/or leek and/or water dropwort, cucumber, carrot and/or carrot juice, onion, green pepper, and zucchini, pumpkin and/or pumpkin juice. Further, fruit and vegetable consumption were summed up. The average intake of fruits and vegetables was estimated using the baseline FFQ and the follow-up FFQ, to represent long-term intake. Participants were then divided into quintiles according to their fruit consumption, vegetable consumption, and fruit and vegetable consumption.

    Definition of NAFLD

    The endpoint of the present study was the occurrence of NAFLD, which was diagnosed based on the results of health examination after the baseline examination but before the follow-up examination. NAFLD was diagnosed based on FLI. FLI has been reported to have high accuracy, based on the area under the receiver operating characteristic curve, in detecting hepatic steatosis.11 FLI was calculated using the following formula: Embedded Image

    Participants with FLI ≥60 were defined as having NAFLD.

    Assessment of other variables

    Sociodemographic variables, including age, sex, educational level and health-related lifestyle variables (alcohol consumption, current smoking status and physical activity), were recorded through self-administered questionnaires. Trained interviewer collected and entered data from survey questionnaires using a standardised method. The entering system is a client/server-based database accessible via internet.24 Data from baseline survey were used for confounding variables. Educational level was classified into three categories: less than middle school, high school and beyond college. Based on alcohol consumption, individuals were classified into two categories: ‘current drinker’ (drank alcohol at the time of survey) and ‘non-drinker’ (never drank alcohol or abstained from alcohol). Based on smoking status, individuals were classified into three categories: ‘current smoker’ (smoked cigarettes at the time of survey), ‘past smoker’ (abstained from cigarette smoking) and ‘never smoker’ (never smoked cigarettes). Finally, based on physical activity, individuals were classified into two categories: ‘active’ (performed physical activity for ≥30 min once daily for ≥5 days a week) and ‘inactive.’ BMI values were used to categorise participants into the following groups: underweight (BMI <18.5 kg/m2), normal weight (BMI ≥18.5 kg/m2 to <23 kg/m2), overweight (BMI ≥23 kg/m2 to <25 kg/m2) and obese (BMI ≥25 kg/m2) according to the International Obesity Task Force Classification for adults in Asian and Pacific regions.27

    Statistical analysis

    For each participant, person-years of follow-up were calculated from the baseline to the follow-up examination. Cox proportional hazards regression analysis was performed to estimate the relative risk (RR) and 95% CI of NAFLD according to the quintile of consumption of the following: fruits, vegetables, total fruits and vegetables, and specific type of fruits and vegetables, after adjusting for potential confounders such as age (continuous), BMI (continuous), educational level, alcohol consumption, smoking status, physical activity, energy intake (continuous), and red and processed meat intake (continuous). All statistical analyses were performed using SAS software version 9.4 (SAS Institute, Cary, NC, USA), and a two-sided p value <0.05 was considered statistically significant.

    RESULTS

    During a median of 4.2 years of follow-up, 2130 incident cases of NAFLD were documented. The general characteristics of the study population at baseline according to the quintile of fruit and vegetable consumption by sex are shown in table 1. Among both men and women, compared with those with lower fruit consumption, participants with higher fruit consumption tended to have a higher educational level, not consume alcohol, not be current smokers and be physically active (all p<0.05). Similarly, compared with those with lower vegetable consumption, both men and women with higher vegetable consumption tended to have a higher educational level and be physically active (all p<0.001).

    View this table:
    Table 1

    General characteristics of the study participants according to the quintile of fruit and vegetable consumption by sex*

    Participants’ nutrient intakes according to the quintile of fruit and vegetable consumption are shown in table 2. Fruit and vegetable consumption was positively associated with total energy intake, percentage of energy from protein and fat, and cholesterol intake, and these associations became more evident with increasing vegetable consumption than with increasing fruit consumption (all p<0.0001).

    View this table:
    Table 2

    Nutrient intakes of participants according to the quintile of fruit and vegetable consumption by sex

    Table 3 displays the RRs of NAFLD according to the quintile of consumption of fruits, vegetables, and total fruits and vegetables by sex. The median intakes of fruits, vegetables, and total fruits and vegetables in the highest consumption group was four to seven times higher than those of the lowest consumption group (men: Q1 43.0 g/day vs Q5 308.4 g/day for fruits; Q1 41.6 g/day vs Q5 180.5 g/day for vegetables; Q1 108.2 g/day vs Q5 458.8 g/day for total fruits and vegetables; women: Q1 63.9 g/day vs Q5 383.1 g/day for fruits; Q1 47.9 g/day vs Q5 197.2 g/day for vegetables; Q1 139.9 g/day vs Q5 546.8 g/day for total fruits and vegetables). The RRs for NAFLD among women with the highest consumption of fruits and vegetables were 0.77 (95% CI 0.62 to 0.96, p for trend =0.0106) and 0.71 (95% CI 0.56 to 0.88, p for trend =0.0071), respectively, after adjusting for age, educational level, alcohol consumption, smoking status, physical activity, energy intake, red and processed meat intake, and BMI in comparison with those for individuals with the lowest consumption. In men, NAFLD risk tended to decrease with the increased consumption of vegetables (p for trend =0.0374). Regarding the total intake of fruits and vegetables, the RRs for NAFLD were significantly lower in the highest fruit and vegetable consumption group (RR 0.75, 95% CI 0.62 to 0.92, p for trend =0.0047 in men; RR 0.74, 95% CI 0.59 to 0.93, p for trend =0.0021 in women) than in the lowest consumption group.

    View this table:
    Table 3

    Relative risks and 95% CIs of non-alcoholic fatty liver disease according to the quintile of fruit and vegetable consumption by sex

    Table 4 shows the results of additional analyses for specific types of fruits and vegetables. Among fruits, the highest consumption of banana (RR 0.75, 95% CI 0.63 to 0.90 in men; RR 0.78, 95% CI 0.63 to 0.97 in women), persimmon (RR 0.82, 95% CI 0.69 to 0.99 in men; RR 0.77, 95% CI 0.63 to 0.94 in women) and apple/apple juice (RR 0.72, 95% CI 0.59 to 0.88 in men; RR 0.79, 95% CI 0.64 to 0.97 in women) was associated with lower risk of NAFLD in both men and women in comparison with those with the lowest consumption. Among vegetables, Korean cabbages (RR 0.79, 95% CI 0.66 to 0.95 in men; RR 0.78, 95% CI 0.63 to 0.96 in women), spinach (RR 0.72, 95% CI 0.59 to 0.87 in men; RR 0.76, 95% CI 0.62 to 0.93 in women), other green vegetables (RR 0.63, 95% CI 0.52 to 0.77 in men; RR 0.77, 95% CI 0.63 to 0.95 in women), deoduck/doraji (RR 0.67, 95% CI 0.55 to 0.80 in men; RR 0.62, 95% CI 0.50 to 0.76 in women), oyster mushroom (RR 0.73, 95% CI 0.61 to 0.88 in men; RR 0.71, 95% CI 0.57 to 0.87 in women), pepper leaves/chamnamul/Aster scaber (RR 0.78, 95% CI 0.65 to 0.94 in men; RR 0.79, 95% CI 0.65 to 0.97 in women), crown daisy/leek/water dropwort (RR 0.81, 95% CI 0.67 to 0.97 in men; RR 0.66, 95% CI 0.53 to 0.82 in women) and pumpkin (RR 0.71, 95% CI 0.60 to 0.84 in men; RR 0.74, 95% CI 0.61 to 0.90 in women) were associated with lower risk of NAFLD in both men and women in comparison with those with the lowest consumption.

    View this table:
    Table 4

    Relative risks and 95% CIs of non-alcoholic fatty liver disease according to the quintile of specific type of fruit and vegetable consumption by sex

    DISCUSSION

    This prospective cohort study, conducted in a large population sample from Korea, showed that fruit intake and vegetable intake were individually associated with a lower incidence of NAFLD in women. Furthermore, the total intake of fruits and vegetables was associated with a lower incidence of NAFLD in both men and women after 4.2 years of follow-up.

    Prospective studies that have examined the effects of fruit and vegetable consumption on the risk of NAFLD are lacking; the existing studies have reported conflicting results. A cross-sectional study in Japan found no significant association between fruit or vegetable intake and NAFLD.28 However, in a cross-sectional study in Korea and a review of seven observational studies, patients with NAFLD were found to consume significantly less fruits and vegetables than the controls.29 30 Also, a nested case–control study with the Multiethnic Cohort showed that there was a significant inverse trend with increasing fruit intake and NAFLD, but none of the point estimates (OR) were statistically significant.22 Vegetable consumption was reported to be not associated with NAFLD.22 Differences in study populations, research designs and diet assessment methods may have caused these differences.

    The mechanism underlying the potential beneficial effects of fruit and vegetable consumption on the risk of NAFLD has not been fully elucidated; however, this can be explained by reduced energy density through adding them into the diet and the antioxidative activities of various polyphenols and carotenoids in fruits and vegetables. First, accumulating evidence has shown that weight loss, through hypocaloric intake, is the most important factor for the prevention and management of NAFLD.16 17 Low-energy-density diets incorporating fruits and vegetables help lower the energy intake without reducing food volume.31 However, in this study, as fruit and vegetable consumption increased, the total energy intake also increased (table 2); particularly in men, the BMI also increased with increasing fruit and vegetable consumption (table 1). These unexpected associations between fruit and vegetable consumption and total energy intake and BMI levels should be considered in the context of both true-positive and false-positive estimations. In terms of true-positive estimations, people who consume more fruits and vegetables might tend to consume more of other foods as well, sequentially resulting in a high energy intake. In this case, fruit and vegetable consumption may have beneficial effects in the prevention of NAFLD, regardless of the energy intake. In terms of false-positive estimations, it is possible that people with higher energy intakes over-reported the consumption of fruits and vegetables listed in the FFQ. People often over-report their consumption of fruits and vegetables, which are perceived as healthy and socially acceptable foods.32 This over-reporting might be especially magnified in people with excessive caloric intakes. Second, polyphenols, a variety of plant metabolites present in fruits and vegetables, can exert beneficial effects on NAFLD by promoting hepatic lipolysis, inhibiting lipogenesis and protecting against hepatic fibrogenesis.33 A review on the effects of anthocyanins on NAFLD described that anthocyanins may prevent the progression of liver damage related to NAFLD through the inhibition of lipogenesis by reducing sterol regulatory element-binding protein 1c levels, promoting lipolysis by inducing the activity of peroxisome proliferator-activated receptors (PPARα) and reducing oxidative stress.21 Furthermore, another review reported that carotenoids, especially β-carotene and lycopene, have protective effects on NAFLD by modulating intracellular signalling pathways, which influence gene expression and protein translation.20 The results of additional analyses for specific types of fruits and vegetables showed that fruits or vegetables which are high in flavonoids or β-carotene such as persimons, apples, spinach, other green vegetables and pumpkin34 were associated with lower risk of NAFLD (table 4). These antioxidant and anti-inflammatory effects of polyphenols on NAFLD are similar to their effects on other chronic diseases. Numerous studies have found that polyphenols, including a variety of flavonoids and carotenoids, have beneficial effects on other chronic diseases such as type 2 diabetes, dyslipidaemia and CVDs.35 36 The common mechanisms involved in the development and progression of NAFLD and other chronic diseases may explain the prevalence of obesity and MetS as metabolic co-morbidities of NAFLD.

    Fructose, found in fruits and vegetables, has been suspected to contribute to the development of NAFLD and its progression.19 However, the results of the present study found that higher consumption of fruits and vegetables was associated with lower risk of NAFLD. Based on the results of the present study and previous studies, it appears that fructose added to sugar-sweetened beverages or other processed foods, and not natural fructose present in fruits or vegetables, is the main contributor to the development and progression of NAFLD.19 Added fructose in particular (sucrose or high fructose corn syrup) can increase de novo lipogenesis and mitochondrial coupling, leading to oxidative stress, while a high-sugar diet can also induce steatohepatitis.19 In contrast, the naturally existing fructose in fruits and vegetables has no adverse effects on NAFLD and is likely protective against NAFLD and other related diseases such as type 2 diabetes.37 Therefore, the consumption of fruits and vegetables and the limiting of added sugar intake are recommended for the prevention and management of NAFLD. These recommendations have been reflected in several dietary guidelines for the general population. The 2019 American College of Cardiology/American Heart Association guideline for the primary prevention of CVD emphasises the importance of consuming healthy food groups including vegetables and fruits and minimising the intake of added sugars and sweetened beverages.38 Furthermore, the 2015 Dietary Reference Intakes for Koreans recommend that sugar added during cooking and processing of food should account for ≤10% of the total energy intake.39

    To our knowledge, this is the first study to prospectively examine the association of fruit and vegetable (combined and individual) consumption with the risk of NAFLD in Korean adults. The strengths of this study included a large sample size and repeated dietary assessments; this helped us to better represent the participants’ long-term intakes of fruits and vegetables as well as to minimise random measurement errors caused by within-person variations. However, this study has several limitations. First, the quantitative information on fruit and vegetable consumption cannot be free of errors and could have involved bias. People tend to over-report their consumption of fruits and vegetables due to the perception that fruits and vegetables are healthy.32 Furthermore, the FFQ is more appropriate for ranking participants according to their food consumption than for estimating accurate intake.40 Therefore, there is a need for caution when interpreting the results of the quantitative intakes of fruits and vegetables. Second, measurement errors in the NAFLD diagnostic method could not be ruled out. Although the FLI has been validated for various populations,14 15 absolute validity for Koreans cannot be guaranteed. Further research based on more accurate diagnostic methods is needed to investigate the effects of the intakes of various food items on the risks of NAFLD and other related diseases.

    CONCLUSION

    This large-scale prospective study in Korea demonstrated that fruit and vegetable intake was associated with a reduced risk of NAFLD. Furthermore, the total fruit and vegetable intake was associated with reduced NAFLD risk. Fruit and vegetable consumption can protect against NAFLD and associated metabolic co-morbidities such as obesity and MetS.

    What is already known on this subject

    • Accumulating evidence indicates non-alcoholic fatty liver diseases (NAFLD) has strong associations with obesity, metabolic syndrome, most notably cardiovascular disease and type 2 diabetes.

    • Fruits and vegetables consumption has been known to be protective against many chronic diseases, but they are also a major source of fructose, which can increase the risk of NAFLD.

    • Limited information is available regarding the effects of fruits and vegetables on the risk of NAFLD.

    What this study adds

    • This study contributes to previous literature by showing that higher fruit, vegetable, and total fruit and vegetable intakes were associated with reduced NAFLD risk. Fruit and vegetable consumption can protect against NAFLD and associated metabolic co-morbidities among Koreans.

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    Footnotes

    • Contributors S-AK analysed the data and drafted the manuscript. SS designed and supervised the study and reviewed the manuscript. All of the authors approved the final version of the manuscript for publication.

    • Funding This research was supported by the National Research Foundation of Korea (NRF) funded by the Korean government (MSIT) (NRF-2020R1C1C1014286).

    • Competing interests None declared.

    • Patient consent for publication Not required.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Data availability statement Data are available upon reasonable request.