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

Redefining a Healthful Diet: New Results from the Largest Observational Study Ever Conducted on Nutrition and Heart Health Challenge Current Advice

Redefining a Healthful Diet: New Results from the Largest Observational Study Ever Conducted on Nutrition and Heart Health Challenge Current Advice

By Orsolya M. Palacios, RD, PhD and Kevin C. Maki, PhD

Background
Cardiovascular disease is a major cause of morbidity and mortality worldwide.  Its relationship to healthful diet and lifestyle practices has been an area of active research for decades since these represent modifiable behaviors that have the potential to affect cardiovascular disease risk and overall health.  Within dietary recommendations, health authorities advise reducing total and saturated dietary fats while increasing carbohydrates from whole grains, as well as intakes of fruits, vegetables, nuts, seeds and legumes (DGA, 2015). These recommendations are based on studies that have been mostly observational in nature and conducted in high-income countries such as the U.S. and those in Western Europe.  The advice to lower saturated fat intake and replace it with unsaturated fat sources stems largely from the linear relationship between saturated fat intake and a low-density lipoprotein cholesterol (LDL-C) level.  LDL-C is a risk factor for cardiovascular disease, and thus, the working concept is that reducing saturated fat intake reduces LDL-C levels which, in turn, reduce cardiovascular disease risk.  In conjunction with lowering saturated fat intake, health authorities recommend reducing intakes of animal products such as meat and dairy products to accommodate higher intake of plant foods.  However, the advice to increase fruit, vegetable and legume intake also stems from observational studies conducted mainly in high-income nations.  Research on the associations of fruit, vegetable and legume intakes with health outcomes in other nations is sparse and inconclusive.

The dietary habits of populations within wealthy countries are generally one of excess, which significantly differs from the dietary habits of populations in low- and middle-income countries, where intake of certain nutrients, including adequate intake of complete proteins, may be sub-optimal.  Furthermore, dietary habits are strongly rooted in cultural practices, which can also vary greatly among countries, regardless of income status.  Since cardiovascular disease is a leading cause of morbidity and mortality in low- and middle-income countries as well, understanding the link between currently recommended dietary patterns, cardiovascular disease events and/or mortality in more globally-represented populations is crucial in providing accurate and meaningful guidelines for healthful food consumption.

 Methods
The Prospective Urban Rural Epidemiology (PURE) study was conducted to address this topic.  Researchers recruited individuals aged 35 to 70 years of age in 18 low-income, middle-income and high-income countries between January 1, 2003 and March 31, 2013 to participate in the PURE prospective cohort study to assess the association between total mortality and major cardiovascular events and diet choices.  Habitual dietary intake data was analyzed from 135,355 individuals using validated food frequency questionnaires, which documented energy intake from fat (including total, saturated, monounsaturated and polyunsaturated fat), carbohydrate and protein as well as daily intake of fruit, vegetable and legume servings.  Demographic information, socioeconomic status, lifestyle, physical activity, health history and medication use questionnaires were also distributed and assessed.  Trained physicians using standard definitions completed standardized case-report forms to report mortality and major cardiovascular events.  The primary outcomes in this study were total mortality and major cardiovascular events (fatal cardiovascular disease, non-fatal myocardial infarction, stroke and heart failure) and secondary outcomes were all myocardial infractions, stroke, cardiovascular disease mortality, and non-cardiovascular disease mortality.

To assess associations between macronutrient energy contribution and cardiovascular disease events and/or mortality, participants were categorized into quintiles based on the dietary percentage of energy from total fat, individual fats, carbohydrates and protein; hazard ratios (HRs) were calculated using a multivariable Cox frailty model.  To assess the associations between daily fruit, vegetable and legume servings and cardiovascular disease events and/or mortality, Cox frailty models with random effects were also employed and HRs calculated.

Results
Median follow up of participants was 7.4 years during which time 5796 deaths and 4784 major cardiovascular disease events were recorded.  Regarding macronutrient intake, higher carbohydrate intake was associated with a significantly higher total mortality risk for the highest quintile versus the lowest quintile, but there was no significant association between carbohydrate intake and cardiovascular disease, myocardial infarction, stroke or cardiovascular disease mortality.

Results from this study indicate that total fat, as well as saturated, monounsaturated and polyunsaturated fats all were significantly associated with a lower risk of mortality for the highest quintile versus the lowest quintile of total and individual fat intake.  Specifically, the HR for the highest versus the lowest quintile of fat intake was 0.77 (95% confidence interval [CI] 0.67-0.87) for total fat, 0.86 (95% CI 0.76-0.99) for saturated fat, 0.81 (95% CI 0.71-0.92) for monounsaturated fat, and 0.80 (95% CI 0.71-0.89) for polyunsaturated fat.  For cardiovascular disease events, the highest quintile of saturated fat intake was associated with a significantly lower risk of stroke (HR 0.79, 95% CI 0.64-0.98) compared to the lowest quintile of saturated fat intake.  Neither total fat nor any of the individual fats were associated with myocardial infarction risk or cardiovascular disease mortality.

Like total fat, the highest quintile versus the lowest quintile of total protein intake was significantly and inversely associated with total mortality risk (HR 0.88, 95% CI0.77-1.00) and non-cardiovascular disease mortality (HR 0.85, 95% CI 0.73-0.99).  Animal protein intake was associated with a significantly lower risk of total mortality whereas plant protein intake had no significant association with total mortality.

Total Fat HR (5th Quintile vs. 1st Quintile) 95% CI P-trend
Total Mortality 0.77 0·67–0·87 <0.0001
CVD Mortality 0.92 0·72–1·16         0.50
Non-CVD Mortality 0.70 0·60–0·82       <0.0001
Major CVD Events 0.95 0·83–1·08         0.33
Saturated Fat HR (1st Quintile vs. 5th Quintile) 95% CI P-trend
Total Mortality 0.86 0·76–0·99 0.0088
CVD Mortality 0.83 0·65–1·07         0.20
Non-CVD Mortality 0.86 0·73–1·01 0.0108
Major CVD Events 0.95 0·83–1·10         0.49
Fruits, Vegetables & Legumes HR (< 1 serving/day vs. 3-4 servings/day) 95% CI P-trend
Total Mortality 0.78 0.69–0.88 0.0001
CVD Mortality 0.81 0.65–1.02 0.0568
Non-CVD Mortality 0.77 0.66–0.89 0.0038
Major CVD Events 1.06 0.92–1.22 0.1301

Abbreviations: CVD, cardiovascular disease; HR, hazard ratio

Adapted from: Ramsden et al. Lancet (2017) S0140 (17)32241-9; Toledo et al.  Lancet (2017) S0140-6736(17)32251-1.

The mean fruit, vegetable and legume intake was 3.91 (standard deviation 2.77) daily servings.  When the researchers assessed the links between fruit, vegetable and legume intakes and outcomes, they found that higher fruit, vegetable and legume intake was significantly inversely associated with major cardiovascular disease, myocardial infarction, cardiovascular mortality, non-cardiovascular mortality and total mortality after adjustments for age, sex and random effects.  However, these effects were diminished after multivariable adjustments.  The HR for total mortality was lowest for those consuming three to four daily servings of fruit, vegetables and legumes (HR 0.78, 95% CI 0.69-0.88) compared to the reference group, who consumed less than one serving of these foods per day.  Higher intakes of fruits, vegetables and legumes were not associated with further lowering of risk.  When assessed independently, fruit intake was associated with lower mortality, including total mortality, cardiovascular mortality and non-cardiovascular mortality.  Raw vegetables were strongly linked to lower mortality risk whereas cooked vegetables had a modest association with lower risk.  Legume intake was inversely associated with non-cardiovascular death and total mortality.

Comment

To date, the PURE study is the largest observational study to assess the link between nutrient intakes, food group intakes, cardiovascular disease events (including death) and overall mortality.  It encompassed data from over 135,000 participants in 18 countries across five continents from low-, mid- and high-income nations.  The results of this study align with some general recommendations (e.g,. emphasize consumption of fruits, vegetables and legumes) but are in conflict with some others.  For example, health authorities recommend increasing intakes of fruits, vegetables and legumes at the expense of animal foods (DGA, 2015).  However, the results of this study suggest that the association between increased fruit, vegetable and legume intake plateaus after three to four daily servings, and the median fruit, vegetable and legume intake among participants was already 3.9 daily servings.  Thus, as a whole, participants were theoretically obtaining the maximal benefit from intake of these foods and the incremental benefit beyond the median level of intake in the populations studied is uncertain.  The study’s finding that higher energy intake from animal protein is linked to reduced total mortality, while plant proteins, such as those found in legumes, showed no significant association, does not align with the some aspects of the current Dietary Guidelines for Americans (DGA, 2015).  Although it recommends an increase in seafood, The Dietary Guidelines for Americans also recommends strategies such as using legumes, nuts and seeds in place of meat and poultry in mixed dishes to attain protein needs and to increase vegetable intake while cutting back on foods such as some meats, poultry and cheeses to help lower saturated fat intake (DGA, 2015).

However, the PURE study results challenge the emphasis on reducing intake of saturated fat.  Higher energy intake from fat and each individual type of fat, including saturated fat, was associated with lower total mortality, as well as lower risk for some cardiovascular disease events.  Carbohydrate energy intake either showed no association on assessed outcomes or was associated with an increased risk for mortality.  However, it should be emphasized that intakes of saturated fats were generally low, with mean values ranging from 5.7% in China to 10.9% in Europe and North America.  Across countries, total and saturated fat intakes are positively associated with socioeconomic status.  Thus, in countries with higher intakes of total and saturated fat, and thus lower intakes of carbohydrate, higher socioeconomic status, with resulting access to higher quality healthcare, is a potential confounder.

Taken together, the results from PURE raise questions about current dietary guidance, which is largely based on results from observational studies completed in the U.S. and Europe.  Unfortunately, very few randomized, controlled trials have been completed to assess the influence of dietary guidance on long-term health and disease incidence.  While difficult and expensive, these are essential for fully evaluating the potential benefits and risks of dietary recommendations (Maki, 2014).  The strongest recommendations should be limited to those instances where results from randomized, controlled trials align with findings from observational studies.  While the results from PURE are at odds with some current dietary recommendations, they are consistent with the age-old adage “everything in moderation.”

 PURE Study References

Dehghan M, Mente A, Zhang X, et al. Associations of fats and carbohydrate intake with cardiovascular disease and mortality in 18 countries from five continents (PURE): a prospective cohort study.  Lancet. 2017; S0140-6736(17)32252-3.

Miller V, Mente A, Dehghan M, et al. Fruit, vegetable, and legume intake, and cardiovascular disease and deaths in 18 countries (PURE): a prospective cohort study.  Lancet. 2017; S0140-6736(17)32253-5.

Ramsden CE, Domenichiello AF. PURE study challenges the definition of a healthy diet: but key questions remain.  Lancet. 2017; S0140-6736(17)32241-9.

Toledo E, Martinez-Gonzalez MA. Fruits, vegetables, and legumes: sound prevention tools.  Lancet. 2017; S0140-6736(17)32251-1.

Additional References

Maki KC, Slavin JL, Rains TM, Kris-Etherton PM.  Limitations of observational evidence: implications for evidence-based dietary recommendations.  Adv Nutr. 2014;5(1)7-14.

U.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 https://health.gov/dietaryguidelines/2015/guidelines/.

Photo by Eaters Collective

Replacing Refined Carbohydrates with Egg Protein and Unsaturated Fatty Acids Improves Insulin Sensitivity and the Cardiometabolic Profile

Replacing Refined Carbohydrates with Egg Protein

Replacing Refined Carbohydrates with Egg Protein and Unsaturated Fatty Acids Improves Insulin Sensitivity and the Cardiometabolic Profile

Replacing Refined Carbohydrates with Egg Protein and Unsaturated Fatty Acids Improves Insulin Sensitivity and the Cardiometabolic Profile

Consuming a healthful diet and participating in an adequate amount of physical activity are key tools for managing metabolic abnormalities that can increase risk for both cardiovascular disease and type 2 diabetes mellitus.  A growing body of evidence supports the view that a diet high in refined starches and added sugars exacerbates disturbances in carbohydrate (CHO) metabolism.  Replacement of these macronutrients with protein and/or unsaturated fatty acids (UFA) may help to improve the cardiometabolic risk factor profile.  The MB Clinical Research team conducted a trial to evaluate the effects of a combination of egg protein (Epro) and UFA, substituted for refined starches and added sugars, on insulin sensitivity and other cardiometabolic health markers in adults with elevated (≥150 mg/dL) triglycerides (TG).

Participants (11 men, 14 women) with elevated TG were randomly assigned to consume test foods prepared using Epro (~8% of energy) and UFA (~8% of energy) for the Epro/UFA condition, or using refined starch and sugar (~16% of energy) for the CHO condition.  Each diet was low in saturated fat and consumed for 3 weeks in a controlled feeding (all food provided) crossover trial, with a 2-week washout between diets.  Insulin sensitivity, assessed by the Matsuda insulin sensitivity index (MISI), increased 18.1 ± 8.7% from baseline during the Epro/UFA condition, compared to a change of -5.7 ± 6.2% during the CHO condition (p < 0.001). The disposition index, a measure of pancreatic beta-cell function, increased during the Epro/UFA condition compared to the CHO condition (net difference 40%, p = 0.042), and low-density lipoprotein (LDL) peak particle size increased during the Epro/UFA condition compared to the CHO condition (net difference 0.27 nm, p = 0.019).  TG and very low-density lipoprotein cholesterol (VLDL-C) levels were lowered more following the Epro/UFA (~16% differences, p < 0.002) versus the CHO diet condition.  LDL-C was lowered by 9-10% with both diets, compared with baseline, but the response did not differ between diets.

Comment:

Consumption of a low-saturated fat diet, where ~16% of energy from refined starches and added sugars was replaced with Epro and UFA, increased indices of insulin sensitivity and pancreatic beta-cell function, increased LDL peak particle size, and lowered fasting TG and VLDL-C levels in men and women with elevated TG.  The results of this study are consistent with a previous study by our group, where daily consumption of three servings of sugar-sweetened products reduced insulin sensitivity by 18% as assessed by HOMA2-%S compared to a habitual diet baseline, and three daily servings of dairy products produced no change.  Reductions in TG and VLDL-C may benefit cardiometabolic health, and are often accompanied by a shift toward larger, more buoyant LDL particles.  This shift, as observed in the current trial, may result in a less atherogenic LDL particle.  The findings from this trial support the Dietary Guidelines for Americans’ recommendations to limit intake of refined starches and added sugars, and to emphasize UFA intake as replacements for both dietary saturated fatty acids and refined CHO.

References:

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;May 17 [Epub ahead of print]

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. Available at http://jn.nutrition.org/content/145/3/459.full.pdf+html.

U.S. Department of Health and Human Services and U.S. Department of Agriculture. 2015-2020 Dietary Guidelines for Americans 2015-2020. Eighth Edition. December 2015. Available at http://health.gov/dietaryguidelines/2015/guidelines/.

 

Replacing Refined Carbohydrates with Egg Protein