Professor H Douglas Goff, from the Department of Food Science at University of Guelph, discusses how breakfast cereal, served with milk, can reduce postprandial blood glucose.
For countless people around the globe every morning, a bowl of their favourite breakfast cereal topped with milk is their breakfast of choice. Breakfast cereals are a fast and convenient way for consumers to ensure that they have had their daily recommended amount of micronutrients and dietary fibre. The focus of this article is the contribution of milk proteins to the health benefits of cereal.
We have recognised for years that most cereal proteins are deficient in lysine, which is complemented by adding milk to return the essential amino acid balance back to that required for human intake. I have been part of a multi-lab collaboration that has examined the effect of milk proteins on the kinetics of starch degradation and blood glucose rise, blood amino acid profile, hormonal response and satiety following consumption of a ‘cereal plus milk’ breakfast meal. The collaboration, led by Professor Harvey Anderson, involved Canadian scientists from the University of Guelph, University of Toronto, and Université Laval.
We formulated milk products that contained a normal level of protein, or an enhanced level of milk protein by three times, and in each we maintained the normal level of casein to whey proteins (80 casein:20 whey protein) or we modified the ratio to 40 casein:60 whey protein, which simulates the balance of caseins and whey proteins in human milk. We enlisted a group of 32 participants to consume one of the four milks and a water-based control with two servings of an oat-based breakfast cereal (Cheerios) on each of five weekly visits. We did blood sampling over a two-hour period and asked participants to rate their feeling of fullness/return to hunger (satiety) during the 2-hour period. Following that, we offered them an ad libitum pizza meal and measured their food intake to determine the relationship between satiety and subsequent-meal food intake. The results presented here are a summary of this research project1-3 and a discussion of its significance to one of the most common morning breakfast meals in the world.
Milk proteins delay rise in blood glucose following breakfast meal consumption
The protein content of milk is about 3.1%. It is divided between casein proteins, about 80%, and whey proteins, about 20%. The casein proteins in milk are aggregated together into a submicroscopic sphere known as the casein micelle and its ability to continue to aggregate with other micelles forms the basis for the manufacture of yogurt (an acid gel of caseins from the lactic acid produced by fermentation) and curds for cheese making (a gel induced by enzyme addition, usually rennet).
Whey proteins, on the other hand, are soluble proteins. During the cheesemaking process, they remain in the whey, which is drained from the curds, and can be concentrated from the whey to make industrial whey protein isolates. Milk proteins provide a complete balance of essential amino acids. During digestion, the casein micelles also aggregate in the stomach, leading to delayed hydrolysis and absorption. In infant feeding, this is one of the factors that provides satiety and comfort to the infant between feedings. Our research hypothesis was that milk would delay the digestion and absorption of glucose from starch during consumption of a ‘cereal plus milk’ breakfast meal, providing a more balanced blood sugar-time profile and a longer period of satiety, compared to a carbohydrate-rich breakfast in the absence of milk protein.
We recruited 32 healthy, young (18-32), normal body weight (BMI 20.0-24.9) men and women (16 each) for the five-week trial. The breakfast meal consisted of cereal (Cheerios, 58 g, two servings) plus 250 ml of one of five ‘milk’ treatments:
- Normal skim milk, 3.1% protein 80 casein:20 whey protein;
- Modified skim milk with normal protein level, 3.1% 40 casein:60 whey protein;
- Modified skim milk with high protein level, 9.3% 80 casein:20 whey protein;
- Modified skim milk with high protein level, 9.3% 40 casein:60 whey protein; and
- Water plus added lactose and minerals to balance that in the skim milk, as the control.
All of the treatments contained the same carbohydrate content (starch, sugar and lactose). Treatments one and two (430 kCal each) had 60% of the protein coming from milk, 40% from cereal, whereas treatments three and four (500 kCal each) had 80% of the protein coming from milk, 20% from cereal. In the control (400 kCal), all protein was cereal protein.
Blood glucose was measured for two hours after consumption of the breakfast meal. There are several parameters from the blood glucose-time curves that need to be considered during analysis (e.g., peak levels and time to peak, mean change from baseline, area under the curve, etc.). The control sample led to the highest peak in blood glucose at 30 minutes and all of the milk protein treatments resulted in significantly lower levels of blood glucose at 30 and 60 minutes compared to the control. The high protein (9.3%) treatments significantly reduced overall blood glucose concentrations compared to normal protein (3.1%). The effect of casein:whey protein ratio on blood glucose concentration was not as obvious as protein concentration, but when pooled, the 40:60 treatments were slightly, but significantly, lower than the 80:20 treatments.
The first part of the study was therefore clear – milk proteins result in reduced blood sugar levels following consumption of cereal and milk, compared to cereal alone, and the higher the protein, the lower the blood sugar level. Mechanisms could include the effect of the protein on movement of starch from the stomach to the small intestine for hydrolysis and absorption (gastric emptying), a reduction in the rate of starch hydrolysis in the small intestine (from amylase action) leading to slower release of glucose and maltose for absorption (both of these mechanisms are similar to the action of dietary fibre at reducing blood glucose following ingestion of a starch+fibre meal) and/or an increase in insulin secretion induced by the proteins. We sought to verify each of these potential mechanisms.
Gastric emptying
All of the treatments included paracetamol as a marker of gastric emptying. The appearance of paracetamol in the blood is an indicator of how quickly solids are disintegrated and soluble nutrients are released in the watery serum from the stomach. We found that blood paracetamol levels were lower after the treatments containing high versus regular milk protein. However, differences between protein ratios were not obvious. Casein proteins in milk will aggregate under acidic stomach conditions. During digestion, they are known as ‘slow’ proteins in relation to their digestion kinetics and appearance of their amino acids in the blood due to this aggregation. On the other hand, whey proteins are small soluble proteins and move from the stomach quite easily, hence they are known as ‘fast’ proteins in relation to their digestion kinetics. The paracetamol analyses help to show that the presence of milk proteins, particularly the caseins, aid in slowing down the first step of the digestion process of the cereal starch.
The appearance of insulin in the blood to lower absorbed glucose levels is also a significant indicator of the body’s response to the ingested food components. Despite the differences in blood glucose levels, we found that insulin was not affected by protein concentration or ratio, in contrast with the suggestion that lower glucose is due to a rise in blood insulin stimulated by branched-chain amino acids from whey protein digestion. Thus, the reduction in blood glucose in response to the higher levels of milk proteins is insulin-independent and may reflect both the reduced rates of gastric emptying as seen with the paracetamol results and the hormonal response to the proteins, which is further discussed below.
Milk proteins reduced rates of starch digestion
We wanted to look specifically at the effect of milk protein on starch hydrolysis in a simulated in vitro digestion to determine the impact of cereal particle disintegration, viscosity, protein solubility and hydrolysis on the bioaccessibilities of sugars and total amino acids. The normal ratio (80 casein:20 whey) milk treatments demonstrated higher structural retention during the simulated gastric digestion due to the formation of casein aggregates and interaction with cereal components. This corresponded to the slower gastric emptying seen during the human trial. In the simulated small intestinal phase, the higher protein-containing treatments inhibited starch degradation and lowered available sugar levels compared to the control, and this also would have contributed to the lowered blood glucose seen in the human trial, in addition to the reduced gastric emptying. Hence this demonstrates that the simulated in vitro digestion provided similar trends in biomarkers to the human study and can be used to provide clues about specific physiological mechanisms.
Milk proteins modify hormonal response during digestion
During our blood sampling, we measured several hormones to further elicit mechanisms of blood glucose lowering by milk proteins following consumption of the breakfast cereal. We found that plasma C-peptide concentration was not affected by milk protein concentration or ratio. C-peptide is the part of proinsulin that is cleaved before co-secretion with insulin from the pancreatic β cells. This result confirms and further strengthens the results that the blood glucose lowering effect is non-insulin dependent.
Plasma GLP-1 was higher after treatments containing high milk protein and the 40:60 ratio compared with treatments containing regular milk protein concentration and the 80:20 ratio. GLP-1 can induce insulin secretion, and the fact that it showed up in the high whey protein treatments may not be surprising since whey protein has also shown to be insulinemic compared to casein. GLP-1 also slows gastric emptying, which corresponds to our paracetamol results. However, plasma PYY, which also slows gastric emptying, was not affected. Cholecystokinin (CCK) stimulates digestion of protein and also acts to slow gastric emptying. CCK was greater after the high versus the regular milk protein treatments. Although there is some variability in results, the overall message further supports the effect of the milk proteins on reduction in gastric emptying.
Milk proteins increase feelings of satiety after breakfast meal consumption
Pre-lunch appetite (feeling of fullness/return to hunger; satiety) was suppressed to a greater extent with milk beverages that had high (9.3%) compared with regular (3.1%) protein content. However, there were no differences between treatments on lunch meal food intake. It was noted, though, that none of the treatments resulted in a return to baseline of fullness/hunger within the two-hour period before the subsequent meal was served. If that period had been extended to three-to-four hours, as is typically the duration between breakfast and lunchtime meals, any differences between treatments may have become more apparent. There were also some gender differences in caloric intake at the lunchtime meal, with the women showing a significant decrease in food intake with the high whey protein treatments.
Milk and dairy products as part of a healthy diet
Per capita consumption of milk is on the decline in many countries of the world, for a variety of reasons. There are concerns regarding the global environmental impact of animal agriculture and plant-based diets are being heavily promoted. Nevertheless, dairy products in many forms are enjoyed as a source of diversity and pleasure in the diet. The healthfulness of dairy products in the human diet has been well-recognised and dairy has been part of the food guides of many countries for decades. However, there have also recently been many suggestions to the contrary, suggesting people should reduce dairy intake.
Rather than try to open debate on that subject here, I would refer readers to a special issue of Advances in Nutrition (2019)4 in which milk and dairy products in the diet were systematically reviewed in a series of 14 papers for their effects on pregnancy and lactation outcomes; height and bone mineral content in children; all-cause mortality; frailty, sarcopenia and cognitive performance in the elderly; osteoporosis and osteoporotic fractures; metabolic syndrome; Type 2 diabetes; cardiovascular diseases; colorectal cancer; prostate cancer; bladder cancer; inflammatory biomarkers; and cardiometabolic health.
After reading the reviews of thousands of published articles, the editors of the Special Issue concluded, ‘In summary, although there is great heterogeneity in the designs of the studies, all conclude that the consumption of dairy products does not adversely affect mortality. In most cases, regarding the non-communicable diseases included in this supplement, there is a benefit associated with dairy product consumption, sometimes described for total dairy consumption and sometimes for a particular type of dairy product.’4
With regards specifically to Type 2 diabetes (T2D), the chronic disease to which our research is most specifically related, the authors of that review concluded: ‘Total dairy product consumption is associated with a lower risk of T2D, especially for yogurt and low-fat dairy consumption. Moreover, dose–response analyses showed that the risk of T2D decreased by each unit increase in consumption of total dairy products and low-fat dairy products.’5
In the context of breakfast cereal with milk, especially for children, I would like to make one other critical point, and quote again from the above Introductory editorial: ‘The contribution of milk and dairy products as a source of calcium in Western countries is especially noteworthy. Between 50% and 65% of the calcium intake among the population in those countries is provided by dairy products, whereas dairy products only contribute 9–14% of the total energy consumed. Hence, milk and dairy products are nutrient-dense foods that provide high amounts of numerous nutrients (especially calcium) although are relatively low in caloric content.’4 Adequate calcium in the absence of dairy intake is very difficult to achieve, which is of great concern when observing trends in dairy consumption decline.
Conclusions
Our results have demonstrated that milk proteins play an important role in a ‘cereal plus milk’ breakfast meal, not simply by providing its macro- and micronutrients but also by modifying the digestion kinetics of the cereal. Milk proteins lower blood glucose levels associated with digestion of the cereal starch, primarily associated with delayed stomach emptying by a combination of protein aggregation in the stomach and the actions on incretin hormones (CCK, GLP-1) in the small intestine. This effect was seen to be greater with higher protein milk, and to a lesser extent, with higher whey protein:casein ratio.
While the caseins aggregate in the stomach, which leads to reduced gastric emptying, the whey proteins stimulate the digestion-related hormones, which also slow gastric emptying. The combined effect leads to a lower peak in blood glucose and a prolonged absorption period. The observation that the reduced levels of blood sugar are not induced by increased secretion of insulin has enhanced benefits to those individuals with mild insulin resistance and at risk for Type 2 diabetes. Thus, dairy product consumption with meals or before meals may be of benefit to those with insulin resistance for long-term glycemic control. The prolonged digestion process also prolongs the period of satiety between breakfast and lunch, leading to a delayed return of hunger. For the dairy industry, this research has shown potential for enhanced-protein milk beverages, some of which can already be found in the marketplace.
Many people start their day off with cereal and milk as their breakfast meal, likewise many parents start their children’s day off the same way. This research helps to confirm the importance of this daily choice.
Acknowledgements
I would like to acknowledge all of the collaborators to this research program: Bonnie Kung, Amanda Wright, Amy Tucker, Shannon Paré, Dalia El Khoury and all of the research participants at the University of Guelph; Harvey Anderson, project leader, and Shirley Vien at the University of Toronto; and Sylvie Turgeon and Laurie-Eve Rioux at Université Laval, Quebec.
Funding Disclaimer
This research is supported mainly by Agriculture and Agri-Food Canada, and by additional contributions from Dairy Farmers of Canada, the Canadian Dairy Network and the Canadian Dairy Commission under the Agri-Science Clusters Initiative. As per the research agreement, aside from providing financial support, the funders have no role in the design and conduct of the studies, data collection and analysis or interpretation of the data. Researchers maintain independence in conducting their studies, own their data, and report the outcomes, regardless of the results. The decision to publish the findings rests solely with the researchers.
References
- B Kung et al. (2018). ‘Effect of milk protein intake and casein:whey ratio in breakfast meals on postprandial glucose, satiety ratings and subsequent meal intake’. J. Dairy Sci. 101: 8688–8701
- B Kung et al. (2019). ‘Correlating in vitro digestion viscosities and bioaccessible nutrients of milks containing enhanced protein concentration and normal or modified protein ratio to human trial’. Food & Function 10:7687-7696
- D El Khoury et al. (2019). Increased milk protein content and whey-to-casein ratio in milk served with breakfast cereal reduce postprandial glycemia in healthy adults: An examination of mechanisms of action. J. Dairy Sci. 102: 6766-6780
- A Gil and RM Ortega (2019). ‘Introduction and Executive Summary of the Supplement, Role of Milk and Dairy Products in Health and Prevention of Noncommunicable Chronic Diseases: A Series of Systematic Reviews’. Advances in Nutrition, 10 (Suppl. 2, May 2019): S67–S73
- Alveraz-Bueno et al. (2019). ‘Effects of Milk and Dairy Product Consumption on Type 2 Diabetes: Overview of Systematic Reviews and Meta-Analyses’. Advances in Nutrition, 10 (Suppl. 2, May 2019): S154–S163
Professor H Douglas Goff
Department of Food Science
University of Guelph
+1 519 824 4120
dgoff@uoguelph.ca
www.uoguelph.ca/foodscience
Please note, this article will also appear in the second edition of our new quarterly publication.
