Association between Egg Consumption and Metabolic Disease

We searched for past research related with egg consumption and metabolic disease in adults from the earliest available online indexing though December 2017. We identified published articles in PubMed (http://www.ncbi.nlm.nih.gov/pubmed) and EMBASE (http://www.embase.com/). The terms “egg intake”, “egg consumption” combined with “metabolic syndrome”, “CHD”, “CVD ”, and “diabetes mellitus” were used.

We retrieved 46 articles from PubMed and EMBASE. Among them, 20 articles were excluded for one of the following reasons: review articles (n=4), systematic review (n=2), meta-analysis (n=7), case-control study (n=1), or used same subjects in randomized controlled trial (RCT) (n=6). Finally, 26 articles were reviewed: RCT (n=5), prospective study (cohort study) (n=18), and cross-sectional study (n=3).

This study was based on data obtained from the Korea National Health and Nutrition Examination Survey (KNHANES) 2007-2011. This survey was performed by the Korea Centers for Disease Control and Prevention (KCDC). All survey participants signed an informed consent. The KDCD Institutional Review Board (IRB) approved the utilized protocol.

Among 42,347 subjects who participated in the KNHANES survey between 2007 and 2011, we excluded those less than 19 years of age (n=10,635), pregnant/lactating women (n=309), those with missing waist circumference (n=1,928), triglyceride (n=1,271), blood glucose (n=51), blood pressure (n=20) or energy intake data (n=3,414), subjects with unrealistic daily caloric intakes, including <500 or ≥6,000 kcal (n=231) and subjects lacking egg intake frequency data (n=495). Hence, a total of 23,993 subjects were included in the final analysis (9,793 men and 14,200 women).

A diagnosis of MetS was made based on the criteria from the National Cholesterol Education Program Adult Treatment Panel III (NCEP-ATP III). Accordingly, one must possess at least three of the following five components: (1) a waist circumference ≥102 cm (male) or 88 cm (female), (2) blood pressure ≥130/85 mmHg or taking hypertension medicine, (3) a triglyceride (TG) level ≥150 mg/dL or taking medicine for hyperlipidemia, (4) a HDL-C level <40 mg/dL (male) or 50 mg/dL (female), (5) fasting blood glucose >110 mg/dL or taking an antidiabetic drug (Grundy et al., 2004).

Body mass index (BMI) was calculated as weight/height² (kg/m²). We defined obesity as BMI≥25 kg/m², consistent with proposals from the Asia-Pacific region of the World Health Organization (WHO, 2000) and criteria from the KCDC.

Dietary assessment used a qualitative food frequency questionnaire (FFQ) for the past year. The FFQ consisted of a list of 63 commonly-consumed food items in Korea with frequencies of food intake in nine categories (almost never, 6-11 times/year, 1 time/month, 2-3 times/month, 1 time/week, 4-6 times/week, 1 time/day, 2 times/day, and 3 times/day). There were a very small number of subjects who ate three or more eggs per day. Therefore, we re-categorized the frequency of egg intake as ≤1 time/month, >1 time/month – <1 time/week, 1 time/week, 2-3 times/week, 4-6 times/week, 1 time/day, and ≥2 times/day.

The KNHANES has three different parts: a health interview, a health examination, and a nutrition survey. All parts were performed by well-trained medical staff, interviewers, and dieticians. Health examinations such as body measurements, laboratory tests and blood pressure were measured by medical staff. Health interviews and nutrition surveys were conducted via face-to-face interviews. Data for alcohol drinking, smoking, physical activity, and menopause status only were self-reported. More detailed information for measurements of the KNHANES survey is available (Kweon et al., 2014). Sociodemographic information including age, sex, education, and income level were collected via health interviews. With regards to income level, the KCDC provided four categories on the basis of the equivalized income (total household income / the square root of the number of household members). Income level was categorized from 1st (lowest) to 4th (highest) in a dataset provided by the KCDC. Education level was classified into four groups: elementary school, middle school, high school, and college or higher degree.

Alcohol consumption was categorized based on the frequency and amount consumed per occasion. Heavy drinkers were defined as those who consumed alcohol twice or more per week and had at least seven drinks per occasion (for men) or five drinks per occasion (for women). Alcohol intake was classified into non-drinker, less than once a month, more than once a month-less than heavy drinker, and heavy drinkers. Smoking status was classified as non-, past, current (<1 pack per day), or current (≥1 pack per day) smoker. Physical activity was categorized as no exercise, regular walks, regular moderate activity, or regular vigorous activity. Menopausal status was categorized as either yes or no.

Disease history questionnaires were completed using face-to-face interviews. Chronic disease status was dichotomized into subjects diagnosed by physicians with or taking medication(s) for the management of diabetes, cancer, myocardial infarction, stroke, angina pectoris, or chronic renal failure and those without such diagnoses or taking related medications.

Fasting blood glucose, TG, and HDL-C were measured using blood samples collected from subjects in the KNHANES health examination. Systolic blood pressure (SBP) and diastolic blood pressure (DBP) were twice measured by trained nurses. Nutrient intake data such as total energy intake, calcium, and vitamin C intake were obtained from the KNHANES raw data. For further detailed description of the KNHANES, please refer to the official English website (https://knhanes. cdc.go.kr/knhanes/eng/index.do).

Characteristics according to frequency of egg intake in the Korean population were analyzed. Means and standard errors of continuous variables were calculated. The proportions of each covariate for each group were calculated. p-values were calculated using the generalized linear model (GLM)/LSMEAN for continuous variables and Chi-square test for categorical variables. As for the variables with non-normality, we calculated a p-value with log-transformation. Differences between MetS and non-MetS groups were analyzed by t-tests and Chi-square tests for continuous variables and categorical variables, respectively.

We conducted weighted logistic regression to assess the association between frequency of egg intake and MetS. Odds ratio (OR) and 95% confidence interval were calculated. All covariates with a p-value <0.20 in univariate analysis were selected for multiple regression analyses. The multivariate models were adjusted for age, sex, BMI (continuous), income, education, alcohol consumption, smoking status, physical activity, menopausal status (women only), energy intake (continuous) and chronic disease status (yes or no). In addition, we examined the association between egg intake frequency and each component of MetS (abdominal obesity, hypertension, hyperglyceridemia, hypertriglyceridemia, and low HDL cholesterolemia). Tests of linear trend across egg intake frequency were conducted by assigning a median to each frequency and treating it as a continuous variable. All statistical tests were two-tailed and a p-value of <0.05 was considered statistically significant. All analyses were used SAS 9.4 (SAS institute Inc., USA).

Table 1 showed the association between egg intake and metabolic diseases from the literature review. In most cross-sectional and cohort studies, a negative or null association between egg intake and metabolic diseases was observed. Only one cross-sectional study (Shin et al., 2017) and 2 cohort studies (Virtanen et al., 2015; Woo et al., 2016) reported positive results. However, most RCT showed positive results for metabolic disease in egg consumption. The studies conducted in the USA and other Western countries, where a large amount of eggs are consumed, showed that egg intake has a negative or null impact on metabolic diseases. However, previous studies conducted in Korea have reported that egg intake has a positive effect on metabolic syndrome. Therefore, we conducted the analysis between high egg intake and MetS in Korean adults using a representative national data.

Table 2 showed the characteristics of this study subjects according to the frequency of egg intake. Frequent egg consumers tended to be younger, consumed more vitamin C, and were male. They were also more likely to regularly perform vigorous physical activity, and have a higher level of education. The characteristics of the study population according to the MetS status are shown in Table 3. Subjects without MetS tended to be younger; had a low BMI; consumed more energy, vitamin C, and egg; and were female. They were also more likely to be non-smokers, and have a higher level of education.

Table 4 shows the association of MetS and MetS components according to frequency of egg consumption. In multivariate models, compared to lower intake (≤1 time/week), an egg intake of 4-6 times or 7 times per week was significantly associated with a lower prevalence of MetS (OR=0.82; 95% CI=0.71-0.95 for 4-6 times/week; OR=0.83; 95% CI=0.69-0.99 for 1 time/day). As for each component of MetS, an egg intake of once daily was associated with lower prevalences of abdominal obesity (OR=0.77; 95% CI=0.63-0.96 for 1 time/day), hyperglyceridemia (OR=0.82; 95% CI=0.72-0.93 for 4-6 times/week), hypertriglyceridemia (OR=0.83; 95% CI=0.73-0.95 for 4-6 times/week), and low HDL cholesterolemia (OR=0.79; 95% CI=0.71-0.89 for 4-6 times/week; OR=0.83; 95% CI= 0.73-0.95 for 1 time/day) after adjusting for age, sex, BMI, energy intake, drinking, smoking, physical activity, education, income, chronic disease status, menopausal status (women only), and survey year. Consuming two or more eggs daily was not associated with MetS or MetS components.

Majority of previous studies focused mainly on egg consumption and T2D or CVD and the results were controversial (Djoussé et al., 2010; Hu et al., 1999; Li et al., 2013; Shin et al., 2013). A study of 4,568 African Americans concluded that consumption of five or more eggs per week was associated with a higher prevalence of diabetes mellitus (Smith et al., 2015). The Physicians’ Health Study I (1982-2007) and the Women’s Health Study (1992-2007) indicated that daily egg consumption (≥1 egg/day) was associated with an increased risk for T2D (Djoussé et al., 2009). Similarly, daily egg consumption (≥1 egg/day) was shown to increase heart failure risk by about 30% among Swedish males (Larsson et al., 2015). The China National Nutrition Survey reported that egg consumption of 1>time/day was increased a T2D prevalence (OR=2.28) in women and that plasma triglyceride and total cholesterol levels were significantly higher in women taking two or more eggs per week (Shi et al., 2011).

A Korean study reported that consuming ≥3 eggs per week decreased risk for MetS in middle and elderly Korean living in rural areas (RR=0.46 for men, RR=0.54 for women) (Woo et al., 2016). Moreover, Shin et al. (2017) reported that consumption of more than one egg per day was decreased MetS risk compared to those who consumed <1 egg per week in Korean women (OR=0.70). Unfortunately, a gender-stratified analysis was not carried out in this study as there was only a very small number of subjects in the daily egg intake group.

Egg is a nutrient-dense food containing high-quality protein, vitamins, minerals and several bioactive components such as phospholipids, sphingomyelin, lutein, zeaxanthin, and folate. These components regulate lipid absorption, hepatic lipid metabolism and help to increase HDL-C levels (Blesso et al., 2013c; Blesso, 2015). Although eggs are high in cholesterol, with the exact same egg intake, the response to dietary cholesterol may vary depending on the individual (Austin, 1994; Ballesteros et al., 2015). Pyorala (1987) suggested that individual bodies react differently to the type and amount of dietary cholesterol and to avoid excess accumulation of cholesterol in human bodies, compensation mechanisms such as inhibition of cholesterol synthesis or increase of cholesterol emission may occur. Different results on the association between egg consumption and cardio-metabolic risk were likely due to differences in diet intake patterns across countries. Most Koreans obtain 60% or more of their total energy intake from carbohydrates (https://knhanes.cdc.go.kr/knhanes/eng/index.do) and rice is the staple food. Blood glucose level is easily increased with such dietary habits, which is one of the risk factors for MetS. Although, egg intake has been increasing gradually up to about five times in the past 50 years (4.2 g/day in 1969, 26.3 g/day in 2011) (Ministry of Health and Welfare, 2001; Sook, 2003), egg consumption of Koreans remains lower than that of Americans (26.3 g/day in Korea vs. 40.5 g/day in the USA in 2011, respectively). Thus, the effect of egg cholesterol on MetS could be less than that for Western countries.

A recent study suggests that eggs can be used as part of a healthy diet in both the general population and the CVD risk group (Fuller et al., 2015b). Moreover, the World Health Organization (WHO, 2002) has reported that it is not necessary to limit egg yolk intake if fat and meat intake are controlled.

Our study has several strengths. First, this study is the first to evaluate the association between the consumption of two or more eggs per day and MetS in Korean adults. Secondly, our data is from a national sample of Korean adult population. Furthermore, there may have been less measurement errors because anthropometric data were measured using standardized equipment by well-trained health-care professionals.

One of the limitations of our study was that the data was obtained from a cross-sectional survey; hence, a causal-relationship cannot be proven and the effect of confounders cannot be completely eliminated even though the results of this study were adjusted for potential confounding factors. In addition, unintentional bias, such as recall errors may exist since the KNHANES nutrition survey is dependent on the subjects’ memory and honesty.