Healthy adult vegetarians have better renal function than matched omnivores: a cross-sectional study in China

A total of 538 young (34.5 ± 8.7 years) healthy Chinese adults including 269 vegetarians and 269 sex- and age-matched (± 1 year) omnivores were recruited for this study through online and offline approaches. All subjects were volunteers. The vegetarian subjects were recruited through advertisements with the Vegetarian Society of China, some vegetarian restaurants in Shanghai or other publicity in media, and word of mouth. Once included in our study, the vegetarian subjects were asked to recommended one matched omnivore among her or his friends according to the following criteria: 1) the same sex; 2) the same age or ± 1 year; and 3) a similar lifestyle and social class. The recruitment criteria for participants included 1) adoption of a vegetarian diet for at least 12 months (for vegetarians); 2) residence in Shanghai for more than 6 months; 3) age between 18 and 60 years; 4) the ability to understand the contents of the questionnaires; and 5) no history of pregnancy or breastfeeding within the previous 12 months (for female participants). The exclusion criteria included 1) a diagnosis of any renal disease, acute illness and severe nutritional malabsorption. All the subjects were invited to Xinhua Hospital between March 2015 and May 2016 to participate in this study (see the flowchart in Fig. 1) after providing written informed consent. The study was approved by the Ethics Committee of Shanghai Jiao Tong University, School of Medicine.

After 10–12 h of fasting, venous blood was collected from each participant and then sent to the Clinical Laboratory Center of Shanghai Xinhua Hospital for laboratory tests. Data for fasting blood glucose, blood lipid profiles, including total cholesterol (TC), triglycerides (TGs), low-density lipoprotein cholesterol (LDL), high-density lipoprotein cholesterol (HDL), and the LDL/HDL ratio, and renal function parameters, including blood urea nitrogen (BUN), serum creatinine (SCr), and uric acid (UA), were collected. The eGFR was used to evaluate renal function in terms of excretion and filtration and was calculated based on the Chronic Kidney Disease Epidemiology Collaboration (CKD-EPI) from SCr. Higher eGFR values indicate better renal function, mild renal impairment was defined by an eGFR< 90 mL/minute/1.73 m², and the presence of CKD was defined as an eGFR< 60 mL/minute/1.73 m² [16]. Blood pressure was also measured by an automatic blood pressure machine (OMRON, HEM-759P, Japan).

Habitual dietary intakes were assessed in a face-to-face interview using a 24-h recall questionnaire conducted by trained dietitians (The details and of 24 h dietary recall process and questionnaire see the supplement file 1adn 2). We used the 24-h dietary recall questionnaire from “Dietary survey method part of Sanitary Industry Standards of the People’s Republic of China(WST426.1—2013)”, which was widely used in China, including “Chinese National Nutrition and Health Survey” [17, 18]. To help subjects recall and estimate their dietary intakes, dietitians provided food images, oral descriptions, and food models as a part of the 24-h dietary recall method. Data entry and calculation of the 24-h dietary recall questionnaire results were performed using Nutrition Calculator v2.5 software developed by the Institute for Nutrition and Food Safety of the Chinese Center for Disease Control and Prevention and Beijing B-win Technology Co., Ltd.

All vegetarians in our study claimed that they had followed a vegetarian diet by consuming no meat, poultry or aquatic products at any meals daily for over a year. Those who did not consume any animal products were defined as “vegans”, while those who consumed eggs and/or dairy products were considered “lacto-ovo vegetarians”. Among the 269 vegetarians, 70 vegans (26.0%) and 199 lacto-ovo vegetarians (74.0%) were noted. Subjects who did not reject consumption of animal products were defined as omnivores.

All participants were required to complete general condition questionnaires via face-to-face interviews. Basic characteristics such as age, sex, income, education level, marital status, tobacco use, alcohol consumption, work intensity, and the frequency, time, and type of physical activity were recorded.

Height and weight were measured using digital scales to calculate the BMI. We also used a body composition analyzer (Biospace InBody 720, Korea) to detect muscle mass to identify body protein components that could affect renal function indicators, such as creatinine. All the measurements were performed by professional dietitians while the subjects were minimally clothed without shoes.

Data analysis was performed using the Statistical Program for Social Sciences 25.0 (SPSS, IBM, USA). Continuous variables are presented as the means ± standard deviations (SDs) (e.g., age, physical activity, sedentary time, BMI, blood pressure, alcohol consumption, TC, TG, LDL, HDL, the LDL/HDL ratio, BUN, SCr, UA, the eGFR and daily dietary intakes including energy, protein, protein intake/weight, the protein energy supply ratio, calcium, phosphorus, potassium and sodium). Categorical variables (e.g., sex, marital status, regular physical examination, ethnicity, education level, working intensity, income, alcohol use, and mild eGFR impairment) were presented by proportions. To compare differences between the vegetarian group and omnivore group, paired t tests were performed for continuous data, Wilcoxon matched-pairs signed-ranks tests were performed for ordinal variables, and McNemar tests were performed for matched categorical variables. Differences between the vegan group and lacto-ovo vegetarian group were also assessed. We performed two-independent-sample t tests for continuous data and used Wilcoxon rank-sum tests for ordinal variables. χ² tests were performed for categorical variables.

Multivariable-adjusted β coefficients [95% confidence intervals (CIs)] for the associations of vegetarian dietary patterns [omnivore (reference), total vegetarian (lacto-ovo vegetarian and vegan), lacto-ovo vegetarian, and vegan] with renal function parameters (BUN, SCr, UA, and the eGFR) were estimated using linear regression. The covariates were sex, age, BMI, skeletal muscle mass, physical activity, alcohol consumption, smoking status, blood pressure, blood lipid profiles, fasting blood glucose and vegetarian diet duration. The associations between dietary intake compositions and renal function parameters were also estimated using multiple-linear regression. The covariates were sex, age, BMI, skeletal muscle mass, physical activity, alcohol consumption, smoking status, blood pressure, blood lipid profiles, fasting blood glucose and vegetarian diet duration.

All P values were calculated based on two-sided tests, and the significance level for each test was set at P < 0.05.

The basic characteristics of the study participants are shown in Table 1. In our study, the mean age of the vegetarians was 35.4 ± 8.6 years, and the mean duration of vegetarian dietary habits was 5.4 ± 5.0 years. The proportion of alcohol users was lower in the vegetarian group, and the vegetarian group was characterized by lower consumption of alcohol. Vegetarians spent more time being physically active (1.9 ± 2.5 h/week vs. 1.4 ± 2.0 h/week) and tended to have a lower BMI (20.9 ± 2.6 kg/m² vs. 22.4 ± 3.5 kg/m²) and a higher skeletal muscle mass (22.3 ± 4.1 kg vs. 23.3 ± 4.8 kg). Compared with omnivores, vegetarians had a lower systolic blood pressure (108.0 ± 12.7 mmHg vs. 111.6 ± 15.4 mmHg) and lower fasting blood glucose (4.6 ± 0.6 mmol/L vs. 4.8 ± 0.4 mmol/L) as well as better blood lipid profiles, including lower levels of TC and LDL at 4.1 ± 0.8 mmol/L and 2.5 ± 0.6 mmol/L, respectively, and lower LDL/HDL ratios (2.1 ± 0.6 vs. 2.2 ± 0.7).

Table 2 details the daily dietary intake of nutrients of the participants conforming to each of the different dietary patterns. The 24-h dietary recall results demonstrated a significant difference between vegetarians and omnivores. The dietary structure of vegetarians was characterized by lower energy intake (1501.1 ± 514.2 kcal/d vs. 1757.3 ± 588.9 kcal/d), lower energy supply ratios of protein and fat intake (protein: 12.2 ± 3.2% vs. 15.7 ± 4.3%; fat: 25.48 ± 8.60% vs 33.01 ± 9.93%), and a higher energy supply ratio of carbohydrate intake (60.49 ± 9.66% vs. 49.94 ± 11.85%). In addition, dietary fiber consumption was higher among vegetarians, especially vegans. Regarding mineral substances, vegetarians consumed less dietary calcium, phosphorus and sodium than omnivores (all P values < 0.05). Among vegetarians, vegans consumed more dietary energy and protein and had a higher intake of calcium and phosphorus but a lower intake of sodium than lacto-ovo vegetarians (all P values < 0.05).

Figure 2 demonstrates the renal function parameters of omnivores and vegetarians. No subjects had been diagnosed with CKD, and the proportion of mild eGFR impairment was not different between vegetarians and omnivores (13.8% vs. 11.2%) or within vegetarians. The eGFR was higher in vegetarians (109.2 ± 16.6 mL/minute/1.73 m²) than in omnivores (106.2 ± 16.4 mL/minute/1.73 m²). Vegetarians also had lower levels of BUN (3.6 ± 1.0 mmol/L vs. 4.7 ± 5.9 mmol/L), SCr (67.8 ± 10.0 μmol/L vs. 69.5 ± 12.1 μmol/L) and UA (254.6 ± 62.9 μmol/L vs. 272.5 ± 64.3 μmol/L), which are the final metabolites and the representative parameters of renal excretion and filtration. Among vegetarians, the renal function parameters showed no differences between the vegan and lacto-ovo vegetarian groups.

As shown in Table 3, we designed five multiple-linear regression models to explore associations between vegetarian dietary patterns and renal function parameters. In a multiple-linear regression analysis using an unadjusted model, a vegetarian diet was associated with lower BUN [β = − 0.71, 95% CI: (− 0.88, − 0.53)], lower SCr [β = − 1.91, 95% CI: (− 3.72, − 0.10)], lower UA [β = − 18.41, 95% CI: (− 29.11, − 7.70)] and a higher eGFR [β = 3.06, 95% CI: (0.26, 5.85)]. After adjusting for sex, age, BMI and skeletal muscle mass, a vegetarian diet was associated with lower BUN [β = − 0.68, 95% CI: (− 0.85, − 0.51)], lower SCr [β = − 2.04, 95% CI: (− 3.51, − 0.57)], lower UA [β = − 10.17, 95% CI: (− 19.28, − 1.05)] and a higher eGFR [β = 3.59, 95% CI: (0.92, 6.28)]. In model 3, physical activity, alcohol consumption and smoking status were also controlled in addition to the variables included in model 2. After adjusting for LDL and HDL, systolic blood pressure and fasting blood glucose in model 4, a vegetarian diet was negatively associated with BUN [β = − 0.63, 95% CI: (− 0.88, − 0.38)], SCr [β = − 2.04, 95% CI: (− 4.10, 0.02)], and UA [β = − 15.15, 95% CI: (− 27.81, − 2.50)] and positively associated with the eGFR [β = 4.04, 95% CI: (0.30, 7.78)]. After adjusting for vegetarian diet duration, a vegetarian diet remained significantly associated with lower BUN, SCr, and UA levels and a higher eGFR. In a multiple-linear regression analysis, no associations were found between vegetarian diet duration and renal function parameters. Regarding different types of vegetarian diets, both lacto-ovo vegetarian diets and vegan diets were associated with lower SCr, BUN, and UA levels and significantly positively associated with higher eGFRs after adjusting for different confounders.

We designed a multiple-linear regression model to explore associations between dietary intake composition and renal function parameters. When exploring the contribution of dietary composition to renal function parameters, multiple-linear regression results showed that dietary fiber was significantly negatively associated with BUN [β = − 0.02, 95% CI: (− 0.03, 0.00)], SCr [β = − 0.12, 95% CI: (− 0.23, 0.02)], and UA [β = − 0.70, 95% CI: (− 1.34, − 0.06)] and positively associated with the eGFR [β = 0.22, 95% CI: (0.06, 0.41)]. Energy intake, the fat energy supply ratio, the protein energy supply ratio, and protein intake/weight were positively associated with BUN, and the carbohydrate energy supply ratio was negatively associated with BUN, while no convincing association was found between these factors and SCr, UA and the eGFR. To further explore the contributions of different sources of protein to renal function, we divided dietary protein into plant-sourced protein and animal-sourced protein, and the associations between different sources of protein and renal function have been discussed separately. However, we did not detect any associations between plant-sourced protein vs. animal-sourced protein and renal function parameters.