Abstract
Background:
To investigate the association of dairy consumption with metabolic syndrome (MetS) in a representative sample of Korean adult and elderly population.
Methods:
We used data from the Korea National Health and Nutrition Examination Survey, 2013–2018. A total of 18,206 adults (19–64 years) and 5113 elderly people (≥65 years) were included in the analysis. Dairy product consumption was assessed with a 24-hr dietary recall, and the subjects were divided into three groups based on their total dairy consumption (0, <1, ≥1 serving/day). The primary outcome, MetS, was defined according to the National Cholesterol Education Program Adult Treatment Panel III and the Korean Society for the Study of Obesity.
Results:
After adjusting for covariates, high dairy consumption was associated with 12% lower odds of MetS in adults compared with no dairy consumption [odds ratio (OR) 0.88, 95% confidence interval (CI) 0.78–0.998, P for trend = 0.048]. A similar inverse association was found in adult men (OR 0.84, 95% CI 0.71–0.99), but no significant association was found in adult women (OR 0.93, 95% CI 0.78–1.11). For the elderly, high dairy consumption was associated with 20% lower odds of MetS (OR 0.80, 95% CI 0.65–0.98, P for trend = 0.020); a significant inverse association was shown in elderly women (OR 0.72, 95% CI 0.56–0.94) but not in elderly men (OR 0.93, 95% CI 0.68–1.28).
Conclusion:
Our findings suggest that one or more servings/day of dairy products were associated with lower prevalence of MetS in Korean adult men and elderly women.
Introduction
Metabolic syndrome (MetS) is also known as dysmetabolic syndrome, hypertriglyceridemic waist, insulin resistance syndrome, obesity syndrome, or syndrome X. 1 The MetS is diagnosed as the presence of three or more of the following five components: elevated waist circumference, reduced high-density lipoprotein (HDL) cholesterol, elevated serum triglycerides, elevated fasting glucose, and elevated blood pressure. 2 About 20%–25% of adults worldwide have MetS. 3 The MetS was associated with an increased risk of many chronic diseases, such as cardiovascular disease, type 2 diabetes, 1,3 and various cancers. 4 The incidence of MetS has increased markedly in Korea. 5 With the rapid development of the Korean economy, people have had poor dietary habits, increased energy intake, and decreased physical activity. 5 –7 The lifestyle trends might have a large impact on the risk of MetS and overall health.
Dietary factors play an important role in the risk of MetS. Several meta-analyses reported that dairy consumption was inversely associated with risks of type 2 diabetes, 8,9 hypertension, 10 cardiovascular disease, 11,12 and MetS. 13 According to the 2015 Dietary Reference Intake for Koreans (KDRI), it is recommended that adolescents consume two servings of dairy products per day and adults consume one serving of dairy products daily. 14 Dairy products including milk, yogurt, and cheese are a good source of calcium, high biological value proteins, fatty acids, vitamins, and minerals. 15 Calcium and vitamin D in dairy products have been shown to prevent the incidence of MetS. 16
There have been some studies on dairy product consumption and the risk of MetS in Korean population, but the results were inconsistent. 17 –21 Since the prevalence of MetS varies between men and women, as well as adults and the elderly, 5 it should be taken into account when examining the association of dairy consumption with the risk of MetS. Therefore, we aimed to investigate associations of dairy product consumption with the risk of MetS and its components in a large, nationally representative sample of Korean adult and elderly men and women.
Materials and Methods
Study population
This study was based on the data obtained from the Korea National Health and Nutrition Examination Survey (KNHANES), conducted by the Korea Centers for Disease Control and Prevention (KCDC) under the Korean Ministry of Health and Welfare. The KNHANES uses a stratified, multistage, clustered, and probability sampling design to collect representative data on the health and nutritional status of noninstitutionalized civilians in Korea. There are a total of 47,217 participants in KNHANES VI (2013–2015) and VII (2016–2018), and among them, 39,642 participants completed the health interview, health examination, and nutrition survey. We initially excluded 8453 subjects <19 years old, and then sequentially excluded the following individuals: 2916 subjects who had previously diagnosed with a stroke, myocardial infarction, or cancer; 409 subjects who were pregnant or lactating women; 536 subjects who had extreme total energy intakes (<500 or >5000 kcal/day); 1331 subjects who had no fasting status at blood test; 1164 subjects who had incomplete information on biomarkers; 1514 subjects who had missing data on smoking, alcohol consumption, or moderate or vigorous physical activity. Finally, we included a total of 23,319 subjects (18,206 adults, 5113 elderly people) in this analysis. Informed consent was obtained for each participant in the survey, and the Institutional Review Board of the KCDC provided formal ethics approval for the KNHANES dataset (2013-07CON-03-4C, 2013-12EXP-03-5C, 2018-01-03-P-A).
Dietary assessment
Dairy product consumption was assessed from a 24-hr dietary recall based on the coding scheme of KNHANES. 22,23 According to the KDRI, one serving was defined as 200 grams for milk, 150 grams for liquid yogurt, 100 grams for semisolid yogurt, 20 grams for cheese, and 100 grams for dairy-based desserts. 14 The total dairy consumption was classified as three groups (0, <1, ≥1 serving/day).
Assessment of MetS
The waist circumference of participants was measured by trained researchers to the nearest 0.1 cm. The blood pressure was measured after the participants had rested for 5 min in a sitting position, and all blood pressure measurements were taken three times at 30-sec intervals between readings. The average of the second and third readings of systolic blood pressure and diastolic blood pressure were used for the analyses. The HDL-cholesterol, triglyceride, and fasting plasma glucose were measured using Hitachi Automatic Analyzer 7600 (Hitachi, Japan). The MetS was defined according to the National Cholesterol Education Program Adult Treatment Panel III (NCEP ATP III) 24 and the Korean Society for the Study of Obesity 25 criteria. Participants were diagnosed with MetS when they were diagnosed with at least three of the following five components: (1) abdominal obesity (waist circumference ≥90 cm in men and ≥85 cm in women); (2) elevated blood pressure (systolic blood pressure ≥130 mmHg or diastolic blood pressure ≥85 mmHg or use of antihypertensive medication); (3) low HDL-cholesterol (fasting HDL-cholesterol <40 mg/dL in men and <50 mg/dL in women); (4) hypertriglyceridemia (fasting triglyceride ≥150 mg/dL); and (5) hyperglycemia (fasting plasma glucose ≥100 mg/dL or use of insulin or oral antidiabetic medication or physician's diagnosis).
Covariates
The demographic and lifestyle factors included age, sex, socioeconomic status, smoking status, alcohol consumption, and physical activity. Education levels were categorized into “middle school or lower,” “high school,” and “college or higher.” Household income levels were categorized into the lowest, lower middle, upper middle, and highest. Smoking status was classified as nonsmoker, former smoker, and current smoker. We surveyed drinking experience in the past year, and alcohol consumption was divided into never/rarely, 1–4 times/month, and ≥2 times/week. Physical activity was assessed through the practice of aerobic activity. The practice of aerobic activity was as follows: ≥150 min/week of moderate physical activity, ≥75 min/week of vigorous physical activity, or ≥150 min/week of a combination of moderate and vigorous physical activity (1 min of vigorous physical activity was considered 2 min of moderate physical activity). In addition, total energy intake was calculated and used as a continuous variable.
Statistical analysis
All statistical analyses were performed using SAS statistical analysis software, version 9.4 (SAS Institute, Inc., Cary, NC). We have combined the data from 2013 to 2018, considering the cluster sampling design for the survey. The general characteristics of the participants were described as continuous variables for body mass index (BMI, kg/m2), total energy intake, nutrient intake, and each type of dairy product intake, and they were expressed as means and standard errors. For categorical variables such as sex, education level, household income, smoking status, alcohol consumption, and physical activity, they were expressed as numbers of subjects and percentages. To evaluate the differences in characteristics among the categories of dairy consumption, we used the PROC SURVEYREG procedure for continuous variables and the chi-square test for categorical variables. Logistic regression analysis using the PROC SURVEYLOGISTIC procedure was performed to estimate the odds ratios (ORs) and 95% confidence intervals (CIs) of MetS according to the categories of total dairy consumption after adjusting for potential confounders in the multivariable models. A two-tailed P value <0.05 was considered to indicate statistical significance.
Results
General characteristics of the study population
The general characteristics of adults and elderly people according to total dairy consumption are shown in Tables 1 and 2. More than half of the population did not consume dairy products. Compared with nondairy consumers, participants who consumed higher levels of dairy products were more likely to be younger both in adults and in the elderly. For adult men and women, frequent dairy consumers were more likely to be nonsmokers, fewer alcohol drinkers, physically active, highly educated, and have higher household income. For elderly men and women, people who consumed higher levels of dairy products were more likely to be physically active, highly educated, have higher household income, and be nonsmokers only for elderly men.
General Characteristics of the Study Subjects According to Total Dairy Consumption in Korean Adults Aged 19–64 Years
Physical activity was defined as ≥150 min/week of moderate physical activity, ≥75 min/week of vigorous physical activity, or ≥150 min/week of a combination of moderate and vigorous physical activity (1 min of vigorous physical activity was considered 2 min of moderate physical activity).
Adjusted for age (continuous), body mass index (continuous), education (less than or equal to middle school, high school, or greater than or equal to college), household income (lowest, lower middle, upper middle, or highest), smoking (nonsmoker, former smoker, or current smoker), alcohol consumption (never/rarely, 1–4/month, or ≥2/week), and physical activity (yes or no).
Further adjusted for total energy intake (continuous).
SE, standard error.
General Characteristics of the Study Subjects According to Total Dairy Consumption in Korean Elderly Aged ≥65 Years
Physical activity was defined as ≥150 min/week of moderate physical activity, ≥75 min/week of vigorous physical activity, or ≥150 min/week of a combination of moderate and vigorous physical activity (1 min of vigorous physical activity was considered 2 min of moderate physical activity).
Adjusted for age (continuous), body mass index (continuous), education (less than or equal to middle school, high school, or greater than or equal to college), household income (lowest, lower middle, upper middle, or highest), smoking (nonsmoker, former smoker, or current smoker), alcohol consumption (never/rarely, 1–4/month, or ≥2/week), and physical activity (yes or no).
Further adjusted for total energy intake (continuous).
The adults and elderly people who consumed higher levels of dairy products also had higher energy and calcium intake than nondairy consumers. For the adult and elderly women, frequent dairy consumers had higher proportion of total energy intake from protein and fat, but had lower proportion of total energy intake from carbohydrate. For the adult and elderly men, frequent dairy consumers had higher proportion of total energy intake from fat, but there was no significant correlation between dairy consumption and energy intake from carbohydrate or protein.
Dairy consumption and MetS in adults and elderly
The associations between total dairy consumption and the risk of MetS in adults are presented in Table 3. Compared with no dairy consumption, high consumption (≥1 serving/day) was significantly associated with lower prevalence of MetS (OR 0.88; 95% CI 0.78–0.998, P for trend = 0.048) after adjusting for potential confounders. The inverse association, however, was shown in adult men (OR 0.84, 95% CI, 0.71–0.99, P for trend = 0.040), not in women (OR 0.94, 95% CI 0.78–1.11). For the elderly, compared with no dairy consumption, those who consumed high levels of dairy products (≥1 serving/day) had 20% lower odds of MetS in the multivariable model (OR 0.80, 95% CI 0.65–0.98, P for trend = 0.020) (Table 4). A stronger inverse association was found in elderly women (OR 0.72, 95% CI 0.56–0.94, P for trend = 0.010) but not in elderly men (OR 0.93, 95% CI 0.68–1.28).
Odds Ratios for Metabolic Syndrome According to Total Dairy Consumption in Korean Adults Aged 19–64 Years
Adjusted for age (continuous), sex, body mass index (continuous), education (less than or equal to middle school, high school, or greater than equal to college), household income (lowest, lower middle, upper middle, or highest), smoking (nonsmoker, former smoker, or current smoker), alcohol consumption (never/rarely, 1–4/month, or ≥2/week), physical activity (yes or no), and total energy intake (continuous).
CI, confidence interval; OR, odds ratio.
Odds Ratios for Metabolic Syndrome According to Total Dairy Consumption in Korean Elderly Aged ≥65 Years
Adjusted for age (continuous), sex, body mass index (continuous), education (less than or equal to middle school, high school, or greater than or equal to college), household income (lowest, lower middle, upper middle, or highest), smoking (nonsmoker, former smoker, or current smoker), alcohol consumption (never/rarely, 1–4/month, or ≥2/week), physical activity (yes or no), and total energy (continuous).
Adjusted for age (continuous), body mass index (continuous), education (less than or equal to middle school, high school, or greater than or equal to college), household income (lowest, lower middle, upper middle, or highest), smoking (nonsmoker, former smoker, or current smoker), physical activity (yes or no), and total energy (continuous).
Adjusted for age (continuous), body mass index (continuous), education (less than or equal to middle school, high school, or greater than or equal to college), household income (lowest, lower middle, upper middle, or highest), physical activity (yes or no), and total energy intake (continuous).
The associations of total dairy consumption with individual MetS components in adults and elderly people are shown in Table 5. In adults, high dairy consumption (≥1 serving/day) was significantly associated with lower prevalence of hypertriglyceridemia (OR 0.90, 95% CI 0.81–0.99, P for trend = 0.031) and hyperglycemia (OR 0.89, 95% CI 0.80–0.98, P for trend = 0.016) compared with no dairy consumption. When stratified by sex, the inverse association of high dairy consumption with hypertriglyceridemia was found in adult men only (OR 0.84, 95% CI 0.74–0.96, P for trend = 0.010), and the inverse association with hyperglycemia became less significant in the sex-specific models. In adult women, we found a significant inverse association of high dairy consumption with elevated blood pressure (OR 0.87, 95% CI 0.76–1.00, P for trend = 0.044). For the elderly population, high dairy consumption was inversely associated with low HDL-cholesterol in elderly women, compared with no dairy consumption (OR 0.79, 95% CI 0.63–0.99, P for trend = 0.032). For hypertriglyceridemia, the elderly people who consumed less than one serving/day of dairy products had 26% lower odds of hypertriglyceridemia than those with no dairy consumption (OR 0.74, 95% CI 0.60–0.92), while higher level of dairy consumption did not show a significant association.
Multivariable-Adjusted Odds Ratios for Components of Metabolic Syndrome According to Total Dairy Consumption in Korean Adults and Elderly People
Data are shown as ORs (95% CIs).
Adjusted for age (continuous), sex, body mass index (continuous), education (less than or equal to middle school, high school, or greater than or equal to college), household income (lowest, lower middle, upper middle, or highest), smoking (nonsmoker, former smoker, or current smoker), alcohol consumption (never/rarely, 1–4/month, or ≥2/week), physical activity (yes or no), and total energy intake (continuous).
Adjusted for age (continuous), body mass index (continuous), education (less than or equal to middle school, high school, or greater than or equal to college), household income (lowest, lower middle, upper middle, or highest), smoking (nonsmoker, former smoker, or current smoker), physical activity (yes or no), and total energy intake (continuous).
Adjusted for age (continuous), body mass index (continuous), education (less than or equal to middle school, high school, or greater than or equal to college), household income (lowest, lower middle, upper middle, or highest), physical activity (yes or no), and total energy intake (continuous).
HDL, high-density lipoprotein.
Discussion
In this large nationwide study, we found that total dairy consumption was inversely associated with the prevalence of MetS in Korean adults and elderly. Compared with people with no dairy intake, the adults and the elderly with one or more servings/day of dairy food had 12% and 20% lower prevalence of having the MetS, respectively. By gender, the adult men and elderly women who had one or more servings/day of dairy products had 16% and 28% lower prevalence of the MetS, respectively, compared with those with no dairy consumption. However, there was no significant association between dairy consumption and MetS in the adult women and elderly men.
Our findings are consistent with those from the meta-analysis that dairy consumption of one serving/day was associated with reduced risk of MetS by 12%. However, the study did not report the results by gender or age. There were several studies that examined the associations between dairy consumption and the risk of MetS in Korean population. 17 –21 The studies reported the effect estimates in all adults aged ≥19 years 18,20 or those aged 30–59, 17 40–69, 19,26 and 19–64 years, 21 and no studies reported findings from the elderly population separately. In addition, some studies did not report sex-specific results, 18,19 and one study reported the findings from Korean men only. 20 Some studies showed that total dairy consumption was associated with decreased risk of MetS 17,19,26 in all subjects. By gender, a cohort study with subjects aged 40–69 years showed inverse associations both in men and in women. However, one study with subjects aged 30–59 years showed an inverse association in men only, 17 and the other study with those aged 19–64 years showed an inverse association in women only. 21 One study with male subjects aged ≥20 years reported no significant association with total dairy consumption. 20 In our study, we found an inverse association with the MetS in adult men, but not adult women.
We found that people with high dairy intake also have high calcium intake, mostly from dairy products. The daily calcium intake of nondairy consumers was much lower than the estimated average requirement (EAR) of the KDRI for calcium intake, and people with one or more servings/day of dairy products reached the EAR. Among dairy products consumed by adults and the elderly, milk accounts for the largest proportion, followed by yogurt. The adults consumed dairy products more than the elderly overall, but yogurt consumption was higher in the elderly. In both the adults and the elderly, the more they consumed dairy products, the higher percentage of total energy from fat they had. For low-fat or skimmed milk consumption, the elderly population than the adults, and women than men tended to consume more low-fat or skimmed milk.
Several possible mechanisms suggest that dairy consumption may reduce the prevalence of MetS. Calcium is one of the main ingredients of dairy products, which in many ways affects the risk of MetS. Calcium affects MetS through its effect on serum lipid profile and obesity. 16 Calcium binds to saturated fatty acids or bile acid in the intestinal tract to inhibit its absorption, thereby reducing serum low-density lipoprotein cholesterol. 16,27 In addition, increased calcium intake in the diet reduces the level of 1,25-dihydroxy vitamin D hormone, thereby reducing the absorption of Ca2+ to the cells. 16,28 Decreased intracellular calcium levels stimulate lipolysis and reduce the transcription of fatty acid synthase, which leads to the inhibition of fat production. 16,28 On the contrary, calcium affects MetS through its effect on blood pressure. 16 Calcium intake may regulate blood pressure by modifying intracellular calcium in vascular smooth muscle cells and changing blood vessel volume through the renin–angiotensin–aldosterone system, so low calcium intake would increase blood pressure. 29 Dairy protein in dairy products, mainly including casein and whey protein, also affects MetS. Several previous studies have shown that dairy protein can lower blood pressure. One of the potential mechanisms of the antihypertensive effect of dairy protein was the inhibition of the angiotensin-converting enzyme. 16,30,31 Dairy protein-derived biologically active peptides block the action of angiotensin-converting enzymes, thereby inhibiting the conversion of angiotensin I to angiotensin II in the renin–angiotensin–aldosterone system, thus lowering blood pressure. 16 In addition, many studies have mentioned the potential mechanism of the possible connection between the intake of saturated fatty acids in dairy products and the MetS risk, but there was still a lack of comprehensive explanation of these potential mechanisms. 32
In the adult population of our study, we found an inverse association of MetS in men, but not in women, and a decreased prevalence of hypertriglyceridemia was found in men with high dairy consumption. Previous studies also showed that the consumption of dairy products was associated with reduced risk of hypertriglyceridemia in adult men, but not in women. 17,33 The adult men in our study had relatively high BMI (mean 24.63), while the adult women had a mean BMI of 22.95. A previous study showed that there was a significant inverse association between the intake of dairy products and the prevalence of MetS in obese adult men, but not in normal weight adult men. 20 For the elderly population of our study, we found an inverse association of MetS in women but not in men. The elderly women had relatively high BMI (mean 24.43), and the percentage of total energy from carbohydrates exceeded the KDRI standard (55–65 of energy), while the percentage of total energy from fat was below the KDRI standard (15–30 of energy). The previous study showed that a high carbohydrate diet was associated with high serum triglyceride 34 and low HDL-cholesterol 35 in women. Since the elderly women had a relatively high risk of MetS, the beneficial effects of dairy products may be more pronounced in elderly women. In addition, the elderly women consumed more low-fat or skimmed milk than the elderly men. The previous study showed that low-fat milk reduced the incidence of MetS in the elderly, while whole milk has no significant association. 36
This study has some strengths and limitations. This is the first study to examine the association between dairy consumption and MetS in adults and the elderly separately. There were few studies on the association between dairy consumption and MetS in the elderly population, and no study comprehensively analyzed the associations in Korean adults and the elderly by gender. Since the study used nationally representative data of Korean population, these findings can be generalized to Koreans. Nevertheless, due to the cross-sectional nature of our data, we should be cautious to interpret the causal relationship between dairy consumption and the risk of MetS. In addition, we used data collected from the 24-hr dietary recall, so it could be possible to reflect the short-term intakes rather than usual intakes of the participants. 37
In conclusion, the consumption of one or more servings/day of dairy products was inversely associated with the MetS in Korean adult men and elderly women. Further prospective studies should be conducted to confirm the sex-specific effects of dairy products on MetS in adults and the elderly.
Footnotes
Author Disclosure Statement
No conflicting financial interests exist.
Funding Information
This work was supported by the National Research Foundation of Korea funded by the Korean government (NRF-2018R1D1A1B07045353).
