Comparing the Effects of Consuming Egg-based Breakfast Meals, versus Higher Carbohydrate Breakfast Meals, on Cardiometabolic Risk Factors

Comparing the Effects of Consuming Egg-based Breakfast Meals, versus Higher Carbohydrate Breakfast Meals, on Cardiometabolic Risk Factors

By Mary R Dicklin, PhD and Kevin C Maki, PhD, CLS, FNLA

 

Recently, our group conducted a clinical trial that compared the effects of consuming egg-based breakfast meals with non-egg, higher carbohydrate breakfast meals on cardiometabolic risk factors in overweight or obese adults with prediabetes and/or metabolic syndrome.1  Thirty men and women with a mean age of 54.1 years and mean body mass index of 31.9 kg/m2 incorporated into their habitual diets either breakfast meals containing 2 eggs per day for 6 days per week, or energy-matched, non-egg higher-carbohydrate-based meals, for a 4-week period.  After a 4-week washout, subjects crossed over to the other diet condition for a second 4-week period.  The non-egg breakfast meals had, on average, 25 g higher mean sugar content than the egg breakfasts, and the egg breakfast meals had 19 g higher protein content.  Consumption of 12 eggs/week contributed ~315 mg/d of cholesterol to the diet.  Compared to baseline, dietary cholesterol intake was 128 mg/d lower during the non-egg condition and 232 mg/d higher during the egg condition.  Total daily energy intake from diet record analyses during the egg condition was significantly higher than that reported during the non-egg condition (2145 vs. 1996 kcal), but this difference was determined to be due to the intake of foods other than the study products, and there was no significant difference in weight change between the diet conditions.

The primary outcome variable, an insulin sensitivity index from a short intravenous glucose tolerance test, was not significantly altered by either diet condition, and there were no significant differences between or within diet conditions for most other carbohydrate metabolism indicators.  Homeostasis model insulin resistance increased by 24% from baseline during the non-egg condition and was not significantly altered (1.4% increase) during the egg condition, resulting in a significant difference in response between conditions (p = 0.028 between diet conditions).

Low-density lipoprotein cholesterol (LDL-C) declined less from baseline (-2.9%) during the egg vs. the non-egg condition (-6.0%; p = 0.023 between diet conditions), and systolic blood pressure was reduced by 2.7% during the egg condition but was unchanged during the non-egg condition (p = 0.018 between diet conditions).  There were no other significant differences noted in the cardiometabolic risk factor profile.

These results suggest that there was a neutral or modestly favorable effect of egg intake on insulin sensitivity associated with the replacement of higher carbohydrate, non-egg-based foods by egg-based foods at the breakfast meal.  Prior research from our group showed that partial replacement of carbohydrate with a combination of unsaturated fatty acids and egg protein increased insulin sensitivity by 24%.4  Another study by our group showed that 3 servings/day of sugar-sweetened products reduced insulin sensitivity by 18% (HOMA2-%S) compared to the baseline habitual diet, whereas 3 servings/day of dairy products produced no change.5

The Dietary Guidelines for Americans 2015-2020, unlike previous editions, removed the recommendation to limit dietary cholesterol to <300 mg/d, and did not set a limit on egg consumption in a healthy diet.6,7  The 2018 American Heart Association (AHA)/American College of Cardiology/Multi-society Guideline on the Management of Blood Cholesterol also made no specific recommendations on dietary cholesterol.8  Levels of LDL-C were reduced from baseline during both diet conditions in our study.  However, the decline was larger during the non-egg condition (6.0% vs. 2.9%).  With a difference in daily cholesterol intake of ~360 mg/d, the difference in median LDL-C between conditions was 7 mg, or approximately 1.9 mg/dL per 100 mg/d difference in dietary cholesterol.  This difference is approximately what would have been predicted based on linear meta-regression models developed by our group and others.9,10

A recent Science Advisory from the AHA recommended that healthy individuals can include up to one whole egg or equivalent per day as part of a healthy dietary pattern.11  The results from our study are consistent with this recommendation.  Eggs contain cholesterol, but are also a source of important nutrients including unsaturated fatty acids, high quality protein, vitamin D, carotenoids, and choline.12

 

References

  1. Maki KC, Palacios OM, Kramer MW, Trivedi R, Dicklin MR, Wilcox ML, Maki CE. Effects of substituting eggs for high-carbohydrate breakfast foods on the cardiometabolic risk factor profile in adults at risk for type 2 diabetes mellitus. Eur J Clin Nutr. 2020;E-pub ahead of print.
  2. Gadgil MD, Appel LJ, Yeung E, Anderson CA, Sacks FM, Miller ER, 3rd. The effects of carbohydrate, unsaturated fat, and protein intake on measures of insulin sensitivity: results from the OmniHeart trial. Diabetes Care. 2013;36:1132-1137.
  3. Chiu S, Williams PT, Dawson T, Bergman RN, Stefanovski D, Watkins SM, Krauss RM. Diets high in protein or saturated fat do not affect insulin sensitivity or plasma concentrations of lipids and lipoproteins in overweight and obese adults. J Nutr. 2014;144:1753-1759.
  4. Maki KC, Palacios OM, Lindner E, Nieman KM, Bell M, Sorce J. Replacement of refined starches and added sugars with egg protein and unsaturated fats increases insulin sensitivity and lowers triglycerides in overweight or obese adults with elevated triglycerides. J Nutr. 2017;147:1267-1274.
  5. Maki KC, Nieman KM, Schild AL, Kaden VN, Lawless AL, Kelley KM, Rains TM. Sugar-sweetened product consumption alters glucose homeostasis compared with dairy product consumption in men and women at risk of type 2 diabetes mellitus. J Nutr. 2015;145:459-466.
  6. Dietary Guidelines Advisory Committee. Scientific Report of the 2015 Dietary Guidelines Advisory Committee: Advisory Report of the Secretary of Health and Human Services and the Secretary of Agriculture. U.S. Department of Agriculture, Agricultural Research Service, Washington, DC. Available at: https://health.gov/sites/default/files/2019-09/Scientific-Report-of-the-2015-Dietary-Guidelines-Advisory-Committee.pdf.
  7. S. Department of Health and Human Services and U.S. Department of Agriculture. 2015 – 2020 Dietary Guidelines for Americans. 8th Edition. December 2015. Available at http://health.gov/dietaryguidelines/2015/guidelines/.
  8. Grundy SM, Stone NJ, Bailey AL, Beam C, Birtcher KK, Blumenthal RS, Braun LT, de Ferranti S, Faiella-Tommasino J, Forman DE, Goldberg R, Heidenreich PA, Hlatky MA, Jones DW, Lloyd-Jones D, Lopez-Pajares N, Ndumele CE, Orringer CE, Peralta CA, Saseen JJ, Smith SC, Jr., Sperling L, Virani SS, Yeboah J. 2018 AHA/ACC/AACVPR/AAPA/ABC/ACPM/ADA/AGS/APhA/ASI guideline on the management of blood cholesterol: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. Circulation. 2019;139:e1082-e1143.
  9. Clarke R, Frost C, Collins R, Appleby P, Peto R. Dietary lipids and blood cholesterol: quantitative meta-analysis of metabolic ward studies. BMJ. 1997;314:112-117.
  10. Vincent MJ, Allen B, Palacios OM, Haber LT, Maki KC. Meta-regression analysis of the effects of dietary cholesterol intake on LDL and HDL cholesterol. Am J Clin Nutr. 2019;109:7-16.
  11. Carson JAS, Lichtenstein AH, Anderson CAM, Appel LJ, Kris-Etherton PM, Meyer KA, Petersen K, Polonsky T, Van Horn L; American Heart Association Nutrition Committee of the Council on Lifestyle and Cardiometabolic Health; Council on Arteriosclerosis, Thrombosis and Vascular Biology; Council on Cardiovascular and Stroke Nursing; Council on Clinical Cardiology; Council on Peripheral Vascular Disease; and Stroke Council. Dietary cholesterol and cardiovascular risk: a science advisory from the American Heart Association. Circulation. 2020;141:e39-e53.
  12. US Department of Agriculture, Agricultural Research Service, Nutrient Data Laboratory. USDA National Nutrient Database for Standard Reference, Release 28. Version Current: September 2015, slightly revised May 2016.  Available at: https://www.ars.usda.gov/northeast-area/beltsville-md-bhnrc/beltsville-human-nutrition-research-center/methods-and-application-of-food-composition-laboratory/mafcl-site-pages/sr11-sr28/.

 

Photo by Morgane Perraud

Breakfast Skippers Beware: Newly Published Data on Breakfast Patterns Identifies Association with Atherosclerosis, Independent of Cardiovascular Disease Risk Factors

Breakfast Skippers Beware: Newly Published Data on Breakfast Patterns Identifies Association with Atherosclerosis, Independent of Cardiovascular Disease Risk Factors

Insights from the Progression of Early Subclinical Atherosclerosis (PESA) Study

By Kristen N Smith, PhD, RD, LD; Mary R Dicklin, PhD; Kevin C Maki, PhD

 Background: It is well accepted that a person’s lifestyle may impact markers of overall health. Factors associated with lifestyle may be dependent on cultural, social and psychological practices as they fit into a daily routine. Researchers have paid particular attention to the lifestyle habit of breakfast consumption (or non-consumption) and how it may contribute to disease risk.

Whether or not a person consumes breakfast has correlations to such factors as:

  • Measures of satiety,
  • Daily energy intake,
  • Metabolic efficiency of the diet,
  • Appetite regulation.

The regular omission of breakfast has associations with increased cardiovascular health markers such as obesity, diabetes, and unfavorable lipid profiles. Although there have been studies investigating the impacts of breakfast skipping behaviors with heart disease risk, the current study may be the first to research an association between breakfast patterns and subclinical atherosclerosis. The aim of the Progression of Early Subclinical Atherosclerosis (PESA) study1 was to characterize the association between different breakfast patterns and cardiovascular disease (CVD) risk factors; especially focusing on whether the regular omission of breakfast is associated with subclinical atherosclerosis (noted by investigating the presence of atherosclerotic plaques in the carotid arteries, aorta, and iliofemoral arteries or coronary artery calcium in a population with no previous CVD history).

 Methods: The PESA study is an ongoing observational prospective cohort of 4,082 employees of the Bank Santander Headquarters in Madrid, Spain. Male and female volunteers, aged 40 to 54 years old, were included if they met the following criteria:

  • Free of any CVD or chronic kidney disease,
  • No previous transplant,
  • Did not exceed body mass index (BMI) of 40 kg/m2,
  • Did not have any disease that might affect life expectancy and decrease it to <6 years.

Estimates of usual diet were determined through the use of a computerized questionnaire, which was developed and validated in the Estudio de Nutrición y Riesgo Cardiovascular (ENRICA) study of a Spanish population and contains nutritional information on 861 food items including many typically consumed Spanish meals and dishes. Subjects reported the foods consumed in the past 15 days while also noting specific occasions throughout the day (waking up, breakfast, mid-morning, lunch, mid-afternoon, and dinner). To characterize breakfast patterns, the researchers first utilized the quantitative description of breakfast provided by Timlin and Pereira2: “the first meal of the day that breaks the fast after the longest period of sleep, eaten before the start of daily activities (e.g., errands, travel, work), within 2 h of waking, typically no later than 10:00 in the morning, and an energy level between 20 and 35% of total daily energy need.” Additional input was gathered by application of a qualitative definition of breakfast by O’Neill et al. where breakfast is defined as “a food or beverage from at least one food group, and may be consumed at any location. Coffee, water and nonalcoholic beverages are not included in a food group.”3 Mean energy intake of the subjects in the PESA study was 2,314 kcal/day; three major breakfast groups were identified:

  • <5% total energy intake (EI) = skipping breakfast (SBF)
  • 5 to 20% total EI from breakfast = low-energy breakfast (LBF)
  • >20% total EI from breakfast = high-energy breakfast (HBF)

Anthropometric data were collected and CVD risk factors and metabolic syndrome (MetS) were assessed. The European Society of Cardiology CVD risk assessment tool, the Systematic Coronary Risk Evaluation, was used to assess fatal cardiovascular risk. Additionally, researchers noted variables such as age, gender, marital status, highest educational level, smoking status, diet practices and physical activity. Specific ultrasound equipment was utilized to assess atherosclerotic plaque in multiple vascular areas: bilateral carotid, infrarenal abdominal aorta and iliofemoral arteries. Plaques were defined as “focal protrusion into the arterial lumen of thickness >0.5 mm or >50% of the surrounding intima-media thickness or a diffuse thickness >1.5 mm measured between the media-adventitia and intima-lumen interfaces.” Coronary artery calcium (CAC) was also assessed, and states of atherosclerosis were defined as follows:

 

State of Atherosclerosis Definition
Subclinical atherosclerosis The presence of plaque in the right carotid, left carotid, aorta, right iliofemoral, or left iliofemoral or as the presence of calcium (CAC score > 0) in the coronary arteries
Non-coronary atherosclerosis The presence of plaque in the above areas and excluding CAC
Generalized atherosclerosis Dependent on the number of sites affected with atherosclerosis; 4 to 6 sites affected

 

Results: Of the 4,052 participants, 2.9%, 69.4% and 27.7% fell into the SBF (breakfast skipping), LBF (low-energy breakfast) and HBF (high-energy breakfast) categories, respectively. Compared with HBF and LBF, the SBF group was made up mostly of men, current smokers, subjects who had reportedly changed their diet in the previous year to lose weight, and subjects who consumed their highest energy intake at lunch. Compared with HBF, the LBF subjects were more likely to be men with lower education level and to be current smokers with higher calorie intakes at lunch.

Regarding diet quality, the subjects in the SBF group were most likely to have higher energy, protein (from animal sources) and dietary cholesterol intakes while also having the lowest fiber and carbohydrate intakes and greatest consumption of alcoholic and sugar-sweetened beverages and red meat.  The LBF group (compared with HBF) had higher overall energy, animal protein and cholesterol intakes and lower intakes of sugar and polysaccharides while also having dietary patterns lower in fruits, vegetables, whole grains and olive oil and higher in refined grains, red meat, fast food and precooked meals (as well as lean meat and seafood). The HBF group had the greatest intakes of dietary fiber, fruits and vegetables, whole grains and high-fat dairy.

The cardiometabolic risk marker profile was less favorable in the LBF and SBF groups, including higher levels of waist circumference, BMI, blood pressure, blood lipids and fasting blood glucose. Participants in the SBF group had a greater likelihood of scoring high on the European Society of Cardiology Systematic Coronary Risk Evaluation risk scale. Probabilities of obesity, abdominal obesity, MetS, low high-density lipoprotein cholesterol, and hypertension were significantly greater for the SBF group compared with HBF.  The prevalence values for atherosclerosis (subclinical, non-coronary and generalized) across all PESA subjects were 62.5%, 60.3% and 13.4%, respectively.

The odds ratios (ORs) for subclinical atherosclerosis were significantly elevated in the SBF group compared with the HBF group:

  • Abdominal aorta - OR 1.79, 95% confidence interval (CI) 1.16 to 2.77,
  • Carotid atherosclerotic plaques - OR 1.76, 95% CI 1.17 to 2.65,
  • Iliofemoral plaques - OR 1.72, 95% CI 1.11 to 2.64,
  • Coronary atherosclerosis – OR 1.55, 95% CI 0.97 to 2.46,
  • Non-coronary and generalized atherosclerosis - OR 2.57, 95% CI 1.54 to 4.31.

The participants in the LBF group had greater risk of carotid or iliofemoral atherosclerotic plaques compared with the HBF group (OR 1.21; 95% CI 1.03 to 1.43 and OR 1.17; 95% CI 1.00 to 1.37, respectively).

Comment: The results from the PESA study indicate that regular skipping of breakfast was associated with 1.55- to 2.57-fold higher odds for subclinical atherosclerosis, even after adjustment for traditional CVD risk factors and diet quality. Breakfast skipping behavior was also linked to an overall unhealthy lifestyle (poor overall diet, higher consumption of alcohol and smoking).  Other researchers have also noted these same associations in that skipping breakfast is often associated with smoking4, greater total energy intake5, and noncompliance with “Healthy Eating” recommendations.6

Results from PESA confirm the association between breakfast skipping and an adverse cardiometabolic risk marker profile and further show that breakfast skipping is independently associated with subclinical measures of atherosclerosis.  However, the degree to which this association might be causal vs. reflective of residual confounding due to greater exposure to CVD risk markers over time is uncertain.

Several studies have demonstrated that insulin sensitivity shows diurnal variation.  For example, Saad et al. reported that mean values for an index of insulin sensitivity produced from postprandial responses to identical meals at breakfast, lunch and dinner were 11.2, 7.9 and 8.1 (units = 10-4 dL/kg/min/mU/mL).7  Thus, insulin sensitivity was ~40% higher in the morning compared with the afternoon or evening.  It is possible that consuming a lower percentage of daily energy during the times of day when insulin sensitivity is highest (consumption of a low-energy breakfast or breakfast skipping) has an adverse impact on the cardiometabolic risk profile, increasing risks for both type 2 diabetes mellitus and atherosclerotic CVD, although prospective trials will be needed to investigate this possibility.8

 References

  1. Uzhova I, Fuster V, Fernandez-Ortiz A, et al. The Importance of Breakfast in Atherosclerosis Disease: Insights From the PESA Study. J Am Coll Cardiol. 2017;70(15):1833-1842.
  2. Timlin MT, Pereira MA. Breakfast frequency and quality in the etiology of adult obesity and chronic diseases. Nutr Rev. 2007;65(6 Pt 1):268-281.
  3. O'Neil CE, Byrd-Bredbenner C, Hayes D, Jana L, Klinger SE, Stephenson-Martin S. The role of breakfast in health: definition and criteria for a quality breakfast. J Acad Nutr Diet. 2014;114(12 Suppl):S8-S26.
  4. Nishiyama M, Muto T, Minakawa T, Shibata T. The combined unhealthy behaviors of breakfast skipping and smoking are associated with the prevalence of diabetes mellitus. Tohoku J Exp Med. 2009;218(4):259-264.
  5. van der Heijden AA, Hu FB, Rimm EB, van Dam RM. A prospective study of breakfast consumption and weight gain among U.S. men. Obesity (Silver Spring, Md). 2007;15(10):2463-2469.
  6. Smith TJ, Dotson LE, Young AJ, et al. Eating patterns and leisure-time exercise among active duty military personnel: comparison to the Healthy People objectives. J Acad Nutr Diet. 2013;113(7):907-919.
  7. Saad A, Dalla Man C, et al. Diurnal pattern to insulin secretion and insulin action in healthy individuals. Diabetes. 2012;61(11):2691-2700.
  8. Maki KC, Phillips-Eakley AK, Smith KN. The effects of breakfast consumption and composition on metabolic wellness with a focus on carbohydrate metabolism. Adv Nutr. 2016;7 (Suppl 6):613S-621S.

 

Photo by Brooke Lark