Non-alcoholic fatty liver disease (NAFLD) is a metabolic syndrome characterized by abnormal accumulation of fatty material in the liver (1). NAFLD has become the leading cause of chronic liver disease worldwide, accounting for ~25% of the prevalence (2). More than 30% of the population in the United States is affected by NAFLD (3). The growth rate of NAFLD in China is expected to reach its highest point in 2030 (4). NAFLD is associated with adverse outcomes of liver diseases and chronic conditions such as cardiovascular disease and diabetes, making it significant global health and economic burden (5). The pathogenesis of NAFLD is complex, and metabolic disorder syndromes such as obesity, hypertension, and dyslipidemia are the main causative agents of NAFLD (3). Increasing evidence also suggests that dietary intake plays a vital role in developing NAFLD (6, 7).

High salt intake is a major dietary risk factor, resulting in ~1.8 million deaths worldwide in 2019 (8). A large-scale study of the global impact of diet on health noted that the daily salt intake of the Chinese population exceeds that of other countries and regions (9). Evidence has shown that reducing salt intake can prevent and control obesity and chronic conditions such as hypertension and cardiovascular disease (10). As a result, it is essential to focus on salt intake in the Chinese chronic disease population and analyze its association. Current studies on salt intake are usually conducted by self-perception reports and 24-h urine sodium measurements. Self-perception is less reliable, while 24-h urine sodium measurement is practically difficult to perform and is more suitable for application in small sample sizes (11). Casual spot urine estimation of 24-h urine sodium is the more commonly used method for estimating the level of salt intake in the population (12). Sodium is an essential nutrient for the body, but in asymptomatic adults, higher dietary sodium intake as measured by 24-h urine sodium can increase the development of NAFLD by contributing to obesity (13). Shen et al. (14) found that perceived high salt intake was also associated with a higher risk of NAFLD. However, no studies have directly explored casual spot urine estimates of salt intake and NAFLD in the Chinese population aged 18–59 years.

In addition, since most nutrients may interact with each other in the diet, it is not enough to consider the association of a single nutrient or food with NAFLD (15). Several previous studies have examined various dietary patterns and the risk of NAFLD (16–19). However, little has been reported on the relationship between dietary diversity and NAFLD. Dietary diversity is an essential indicator for evaluating the dietary quality index (20). Being based on food groups is more helpful in predicting nutritional adequacy than individual food indicators, although food groups vary considerably across studies (21). It was proposed that dietary diversity was positively correlated with micronutrient adequacy (22). Besides, a study conducted in Iran showed that higher dietary diversity was associated with higher quality dietary intake (23). It may be thought that subjects with higher quality diets may follow a healthier diet and therefore may be negatively associated with NAFLD. Currently, there is limited evidence, small sample sizes, and inconsistent findings regarding the relationship between dietary diversity and NAFLD, and no studies on dietary diversity and the risk of NAFLD in Chinese populations have been identified.

Salt intake and dietary diversity, as single nutrient and overall dietary quality evaluation indicators, respectively, may be combined to better evaluate the role of dietary factors on NAFLD. Therefore, this study intends to investigate the relationship between salt intake, dietary diversity, and NAFLD in Chinese adults aged 18–59 years by analyzing data from medical examination centers and providing reference evidence for further development of dietary management guidelines for NAFLD.

This study was conducted to understand the relationship between salt intake, dietary diversity, and NAFLD in Chinese adult medical examination adults aged 18–59 years. The results showed that the prevalence of NAFLD among Chinese medical examination adults aged 18–59 years was 32.48%, which was significantly higher than that of a meta-analysis of 256,367 cases on the prevalence of NAFLD in China (20%) (34). In addition, we found that salt intake increased the risk of NAFLD, whereas dietary diversity was a protective factor for NAFLD, and the results were equally stable in the subgroup analysis.

NAFLD is typically a “lifestyle disease,” and the role of modifiable dietary factors in NAFLD is of increasing concern. The imbalance of nutrient intake can easily lead to overweight and obesity, increased blood glucose and lipid levels, and other health risks related to NAFLD (35). Studies have pointed out that dietary therapy can control the absorption of basal state free fatty acids, control postprandial hyperlipidemia, reduce insulin resistance, promote the metabolism and transport of lipoproteins, increase the number of antioxidants in the body, and adjust the dietary structure and balance (36). By preventing or eliminating the causes of fatty liver through reasonable and healthy dietary nutrition, the steatosis of early hepatocytes can be reversed while reducing the patient's symptoms (37). After the development of liver lesions in patients with NAFLD, even with tighter control of risk factors such as BMI, hyperglycemia, and dyslipidemia, only 17.8% of patients eventually reverse their liver lesions to normal (38). Therefore, early screening for dietary factors that can affect NAFLD and targeted prevention is essential to reduce the risk of developing NAFLD.

High salt intake is an essential dietary risk factor for disease burden in the population (39) and has a positive association with obesity, blood pressure, and cardiovascular disease (10, 40). Therefore, it may be associated with the development of NAFLD by the same pathway. Our study found the median and IQR of salt intake in adults aged 18–59 years to be (8.3 [7.1, 9.5]) g/d. This is well above the WHO and FAO recommended daily salt intake of <6 g/d (41). It is also higher than the Norwegian adult population study (8.05 g/d) (42). The results of logistic regression analysis further suggested that salt intake was a risk factor for NAFLD. After controlling for significant confounders in univariate analysis, the results still indicated that increased salt intake increased the risk of NAFLD. Although the mechanisms linking salt intake to NAFLD are unclear, researchers have suggested that insulin resistance may be a metabolic intermediate explaining the relationship between high salt intake and NAFLD (43). A study in rats showed that high salt intake enhances insulin sensitivity in adipocytes, improves glucose uptake and insulin-induced glucose metabolism, and promotes adipocyte hypertrophy (44). In addition, high salt intake activates the aldose reductase-fructokinase pathway in the liver and hypothalamus, leading to obesity, insulin resistance, and NAFLD (45). The significant role of obesity in the development of NAFLD may also be a potential mechanism for the association between salt intake and NAFLD. A high salt diet was found to be independently associated with elevated leptin levels in humans (46), and there was a direct positive correlation between salt intake and BMI or body fat percentage (13). Another study pointed out that high salt can also play a role in hepatic inflammation and fibrosis by modulating the renin-angiotensin system, leading to the progression of NAFLD (47). This provides the supporting basis for the present study. Several previous studies have also found an association between salt and NAFLD. However, the estimation of salt intake is often performed by dietary surveys or 24-h urine sodium assessment rather than the direct calculation of salt intake (11). Spot urine estimation of 24-h urine sodium excretion is considered a simple, rapid, and generalizable method for estimating the level of salt intake in a population (12). This study is the first to analyze the relationship between salt intake and NAFLD by examining spot urine in a large sample of the Chinese medical examination population.

In terms of dietary diversity, participants with NAFLD in this study consumed fewer grains, fruits, milk and dairy products, beans, and more livestock meat, and oils and fats. However, diets that increase the intake of vegetables and fruits, beans, fish and yogurt, and whole grains and reduce foods with meat, salt, and trans fats benefit the organism (48). The Mediterranean diet, characterized by this diet, was associated with lower levels of systemic inflammation and a reduced incidence of NAFLD (49). It is recommended to increase the consumption of grains, fruits, milk and dairy products, and beans and reduce the intake of fats and livestock meats. Several other dietary patterns have been associated with NAFLD. Healthy dietary patterns and Dietary Approaches to Stop Hypertension can play a key role in the prevention and control of NAFLD (6, 16). In a study of Chinese adults, the “Animal Food” dietary pattern of food consumption was associated with an increased risk of NAFLD, and the “Grains-Vegetables” dietary pattern was related to a reduced risk of NAFLD (17). However, it has also been found that a vegetable-rich diet was not associated with NAFLD (18), and the present study also did not find an association between vegetables and NAFLD. In centrally obese adolescents, a Western dietary pattern characterized by consumption of red meat, refined grains, processed meats, and high-sugar beverages may increase the risk of NAFLD (50). A Greek study reported that the fast food-type dietary pattern was independently associated with higher odds of NAFLD due to high levels of C-reactive protein and unsaturated fatty acids (19). A Lebanese study noted that the high fruit diet group was also a major potential risk factor for NAFLD, while the traditional diet consisting of vegetables and legumes was negatively associated with the odds of NAFLD (51). It can be learned that different dietary patterns have different effects on NAFLD, and the evidence focusing on the overall quality of the diet and NAFLD is still weak.

The present study also suggested that dietary diversity, as a protective factor for NAFLD, decreased the risk of NAFLD development. Sufficient DDS was associated with a reduced risk of NAFLD compared to insufficient DDS. Some trial evidence suggested that greater food diversity affected the composition of the gut flora, thereby further improving immune function and health status (52). Previous studies have found that increased dietary diversity reduces the incidence of diseases closely related to NAFLD such as overweight, metabolic syndrome, and cardiovascular disease (31, 53, 54). In addition, higher DDS was related to healthier eating habits and better metabolic profiles. Increased dietary diversity leads to more opportunities to choose foods that are negatively associated with NAFLD. Ebrahimi et al. (55) noted that dietary diversity was correlated with increased vitamin C, calcium, and fiber, all of which were negatively associated with liver disease. Furthermore, dietary diversity may increase the intake of various micronutrients, dietary fiber, and some healthful phytochemicals, which are positively associated with dietary balance (56, 57). A wide variety of foods from the same and different food groups can provide vitamins, minerals, and other micronutrients necessary for the health of the body, thereby improving dietary patterns and optimizing the structure of the diet. The more established “second strike” theory of NAFLD points to the importance of oxidative stress in the development of NAFLD (58). Dietary diversity may increase the adequate intake of antioxidants in the diet (59) and may be associated with NAFLD. Notably, another study found that DDS increase was not significantly associated with NAFLD (15). This difference in results may be due to the inclusion of food groups with different assessment methods, different populations assessed, and smaller samples for dietary diversity in their included studies. Furthermore, dietary diversity is not focused on increasing the number of nutrients but rather on promoting diversity and balance among nutrients. It should be clarified that the dietary diversity of an individual does not indicate complete nutritional health. Dietary diversity can ensure the intake of all types of nutrients, but if a particular nutrient is consumed too much or not enough, it is an unreasonable dietary structure, affecting nutritional health.

This study also showed that NAFLD was related to higher age, considering an association with increased metabolic decrease (38). Men were also prone to NAFLD because they were more socially active in their careers, and many had drinking and smoking habits (35). Consistent with previous studies, NAFLD was linked to overweight/obesity, hyperglycemia, and dyslipidemia, with higher BMI, glucose, and lipids in the NAFLD group than in the control group (35, 58). Alcohol drinking and current smoking were also associated with NAFLD. Evidence has shown that patients with NAFLD should avoid alcohol consumption (60), and passive smoking increases NAFLD risk by ~1.38-fold (61). Conversely, physical activity can improve the metabolic function of all bodies, which helps to control BMI and improve insulin resistance, therefore reducing the incidence of NAFLD (36). In addition, socializing and drinking sugary beverages can also affect NAFLD. Additional socializing can lead to excess nutrients being stored in the liver and the formation of a fatty liver. Sugary beverages can increase the metabolic burden so may be a key driver of NAFLD (62). Interestingly, previous studies suggested a protective effect of meals on time and coffee consumption on NAFLD (63). However, this study found no association between meals on time and coffee consumption and NAFLD in the adjusted regression model. This may be related to other factors, such as different subjects consuming coffee with different types, amounts, and food frequencies. Moreover, the present study found that salt intake was associated with dietary diversity. This has not been described in previous studies. Even without considering the amount and frequency of food intake, a greater variety of food intake can affect salt intake levels. Increased dietary diversity is accompanied by the intake of more categories of foods, which implies that people with sufficient dietary diversity have an increased probability of consuming salt-rich foods. This suggests that in addition to managing single nutrients such as sodium, it is equally important to consider whether the overall dietary intake is balanced for NAFLD (15).

To exclude the effect of these factors on NAFLD, we performed further subgroup analysis that illustrated the stability of the results of this study. The results indicated that salt intake remained a risk factor for NAFLD in all subgroups. This suggests that salt intake must be reduced in the management of patients with NAFLD. The protective effect of dietary diversity on NAFLD was more pronounced in the female, overweight, non-current smoking, non-physical activity, non-socializing, and non-sugary beverage groups. This may be due to the fact that dietary diversity is also influenced by multiple factors. It also reinforces the recommendation that the impact of dietary diversity on the health of different populations of patients with NAFLD should be analyzed on a case-by-case basis.

To our knowledge, this study was the first to examine the relationship between salt intake, dietary diversity, and NAFLD in Chinese adults aged 18–59 years. We obtained the results using data from a large sample of Chinese medical examinations. All data were collected by professionals and quality-controlled to ensure the reliability of the information. We adjusted for multiple confounders in our analysis to build models and performed subgroup analysis to make our results more stable. In addition, our study subjects were the medical examination population, and clinical health care professionals will provide post-test health promotion education and dietary and exercise instructions to these individuals.

This study still had several limitations. First, this was a cross-sectional study, and the results did not reflect causality and the prediction of NAFLD progression, which needs to be further demonstrated in future cohort studies and interventional studies. Second, selection bias needs to be considered, and the population selected for this study was a healthy physical examination population, which may have higher health awareness than other populations. Third, this study evaluated whether the participants had NAFLD and did not assess its severity, which needs to be further explored in future studies. Fourth, the type of food intake in this study was self-reported, it might exist over-reporting and under-reporting situations, thus may causing bias to the results. Besides, the indicator of dietary diversity in this study assessed the variety of foods and did not address the daily energy intake of participants which might be a confounding factor. Finally, we used spot urine to estimate salt intake, and its assessment accuracy may be less than the gold standard.

The prevalence of NAFLD was 32.48% among adults aged 18–59 years in the two Chinese physical examination centers in this study. Salt intake was associated with dietary diversity and NAFLD. Salt intake was an independent risk factor for NAFLD, while a sufficient DDS was a protective factor for NAFLD, and the results were equally stable in the subgroup analysis. It is important to change adverse lifestyle habits and pay attention to the control of salt intake and the balance of dietary diversity in the management of high-risk people to reduce the risk of NAFLD.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The studies involving human participants were reviewed and approved by the Ethics Committee of the Third Xiangya Hospital of Central South University (No. 2020-S587). The patients/participants provided their written informed consent to participate in this study.

XL and YLi: conceptualization, formal analysis, data curation, and methodology. XL, YZ, CZ, LL, and YLu: software, validation, and visualization. YLi and JW: investigation. YLi, JW, and JX: resources. XL: writing—original draft preparation. XL, YD, and JX: writing—review and editing. JW, YD, and JX: supervision and project administration. YD and JX: funding acquisition. All authors have read and agreed to the published version of the manuscript.

This work was supported by the Wisdom Accumulation and Talent Cultivation Project of the Third Xiangya Hospital of Central South University (No. YX202006) and the Special Funding for the Construction of Innovative Provinces in Hunan (No. 2020SK2091).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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