The Implications of Eating or Skipping Breakfast: Physiology, Behavior, and the Satiety Hormone Response
SHAVAWN MARIE FORESTER B.S. (University of California, Davis) 2007 DISSERTATION Submitted in partial satisfaction of the requirements for the degree of DOCTOR OF PHILOSOPHY in Nutritional Biology in the OFFICE OF GRADUATE STUDIES of the UNIVERSITY OF CALIFORNIA DAVIS Approved:
Nancy L. Keim PhD, RD, Chair
Britt Burton-Freeman PhD
Jon J. Ramsey PhD
Committee in charge 2012
i
UMI Number: 3565390
All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion.
UMI 3565390 Published by ProQuest LLC (2013). Copyright in the Dissertation held by the Author. Microform Edition © ProQuest LLC. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code
ProQuest LLC. 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, MI 48106 - 1346
Acknowledgements It is a pleasure to thank my mentor, Nancy L. Keim PhD. Without your encouragement, supervision and support this dissertation would not have been possible. I am grateful for the experience you provided and your welcoming open door policy. You have been a wonderful mentor. To Professor Erwin Bautista PhD and Nancy Hudson M.S. RD, for showing me through example and challenging course work what excellence in teaching truly means. To my grandparents, words will never be enough to thank you for everything you have done for me. You are so much more than just grandparents, you are beautiful people who I love spending time with. You both signify what hard work, dedication, and love can achieve. To my incredible family, you all mean so much to me. Your presence in my life is unquestionable. Thank you for family Easter, river rafting, Thanksgiving, Christmas in Tahoe, and cousin’s weekend; these traditions are part of who I am today. To my best friends, you are irreplaceable! Somehow nothing has changed since we were 12 years old; you are still the funniest people I know. I am so lucky to have you. Also to my amazing friends I have spent the past 5 years with in graduate school, from oral exam practices to mustache parties you all are the biggest contributors to my sustained happiness during the most challenging of times at Davis. Thank you for being yourselves, awesome! To my husband, Chase thank you for always supporting my late nights, crazy schedule, and weeks apart. Thank you for putting life into perspective for me; you were there to celebrate milestones, as well as to help me appreciate the opportunity to learn from disappointment. Thank you for forcing me to celebrate my (our) accomplishments, your laugh and energy I will never
ii
take for granted. Here is to a chapter (or four) in our lives behind us but never forgotten, and to many more adventures and amazing times together. Nobody has been more important to me through my academic pursuits than my mom. Mom thank you for always setting the bar high and providing me with the confidence to peruse all of my hopes, dreams, and goals. This is your accomplishment just as it is mine, so congratulations! We did it!
iii
Table of Contents
page
Acknowledgements…………..……………………………………………………………………ii
Abstract
…………………………………………………………………………………......v
Chapter 1
Further insight into the physiology of breakfast skipping:
A review of the literature……………………………………………………….....1
Appendix 1
……………………………………………………………………………………33
Chapter 2
Habitual breakfast skipping affects fasting insulin resistance…………..……….47
Appendix 2
……………………………………………………………………………………67
Chapter 3
Cognitive perceptions of the breakfast meal: Does meal satisfaction, dietary restraint, and disinhibition affect the satiety hormone response?..........................71
Appendix 3
……………………………………………………………………………….…...91
Chapter 4
Satiety hormone response following a standard lunch in habitual breakfast eaters and skippers……………………………..……………………………….………98
Appendix 4
………………………………………………………………………..…………116
iv
Abstract
Population based descriptive studies, clinical trials, and evidence analysis of the literature have identified regular breakfast consumption as opposed to breakfast omission, as a habit independently associated with a more healthy weight. Recent studies have identified differences in insulin sensitivity and satiety hormones between breakfast eating and skipping groups, which help to explain the association between breakfast consumption and weight regulation. Evaluation of fasting insulin sensitivity, behavior, and the postprandial satiety response between breakfast groups were used to further elucidate the physiologic response to skipping breakfast. First, through a review of the literature the proposed physiologic response to consuming breakfast as well as omitting breakfast is presented. A connection is made between the satiety hormone response and key components of the breakfast meal, which include composition, caloric load, energy density, volume, and time of day. The review findings suggest that breakfast consumption as opposed to breakfast omission stimulates a physiologic response that may help promote a healthy body weight. Chapter 2 examines if self reported habitual breakfast skipping was related to fasting insulin resistance in a sample of 321 adults. Participants completed a questionnaire that focused on eating occurrences throughout the day and were then classified by how frequently they ate breakfast. Breakfast eating was related to fasting insulin and HOMA2-IR, both before and after adjusting for age, sex, BMI, and exercise. These data suggest that fasting insulin resistance is affected by breakfast omission, and supports previous intervention studies that report a decline in postprandial insulin action after breakfast omission.
v
Chapter 3 evaluates the relationship between cognitive perception and the satiety hormone response. In a crossover intervention, satiety hormones (insulin and GLP-1), the hunger hormone ghrelin, and subjective ratings of meal satisfaction and eating behavior were compared before and after a low or high fiber breakfast meal. We found that reported perceptions of meal satisfaction, the perception of the breakfast meal, and the behavioral description of cognitive restraint can influence the physiologic regulation of satiety hormones measured in response to meal ingestion. Further evaluation of food consumption habits should consider cognitive perception as it may be important for optimal satiety and influence food intake regulation. Lastly, chapter 4 was a cross-sectional study to assess the hormones insulin, leptin, GLP-1, and glucagon following a standard lunch meal in 30 women who were habitual breakfast eaters or habitual skippers. We found clear differences in circulating hormones between breakfast eaters and breakfast skippers even though all participants had similar hormone values at the start of the protocol. Our data further support the idea that regularly eating breakfast promotes changes in the postprandial pattern of satiety hormones.
vi
1 Chapter 1 Further insight into the physiology of breakfast: A review of the literature1, 2 Shavawn M. Forester1, Nancy L. Keim1, 2 1
Department of Nutrition, 1 Shields Ave., University California, Davis, CA, USA 95616
2
U.S. Department of Agriculture, Agricultural Research Service, Western Human Nutrition
Research Center, Obesity and Metabolism Research Unit, Davis, CA, USA 95616
2 Abstract The relationship between breakfast and weight has been established through population based descriptive studies, and clinical trials, as well as from evidence analysis of the literature. These descriptive studies show that people who consume breakfast are more likely to have a lower BMI. In addition, they have also identified key components of the breakfast meal that mediate the relationship between eating breakfast and weight regulation such as; meal composition, caloric load, energy density, volume, and time of day. However, few clinical trials have addressed the physiologic link between these components of breakfast and weight regulation. Moreover, only a small number of studies have assessed the physiologic effect of omitting breakfast; and of those, it is difficult to compare their findings because a standard definition for breakfast has not been defined. While there are many factors that contribute to weight maintenance, breakfast consumption as opposed to breakfast omission stimulates a physiologic response that may help promote a healthy body weight. Seeing that breakfast is the first meal of the day, its consumption presents an opportunity to establish a physiologic state conducive to weight maintenance early in the day. The purpose of this review is to present the physiologic response to consuming breakfast as well as omitting breakfast; specifically, we focused on the physiology of the satiety hormone response to breakfast.
3 Introduction Eating breakfast is not a unique habit. The choice to eat healthful foods at the first eating occasion is intuitively thought of as vital for health, a notion shared by cultures and societies throughout the world. The interest in breakfast, as opposed to other meals, has initiated a vast array of investigations. Further, breakfast is an interesting public health issue because the consumption of breakfast is thought to have a beneficial impact on weight regulation. Yet, many Americans do not routinely eat breakfast. According to data collected from National Health and Nutrition Examination Survey (NHANES), breakfast consumption has declined in children, adolescents, and adults despite the common notion that breakfast is a healthy habit 1 . Along with the decline in breakfast consumption, the percent of obese Americans has increased, according to the same NHANES reports 2, 3. Although a direct relationship cannot be determined, the breakfast meal may have a unique influence on food intake and weight regulation as evidenced by the opposing trend between the decreased incidence of eating breakfast and the prevalence of overweight and obesity 4, 5. Breakfast and weight regulation research is complicated due to many uncontrolled, confounding influences. For example, people who eat breakfast are more likely to exercise 6-8 and have an overall better diet quality compared to non breakfast eaters 4, 9, 10. In addition there is no standard definition for breakfast, and as a consequence, previous studies have used many different definitions. A universal definition for breakfast has been difficult to develop because cultural, and social factors, as well as individual opinions must be integrated. In 2008, however, a comprehensive definition of breakfast was proposed in a review article by Timlin et al. The Timlin review defined breakfast as the first meal of the day, eaten before or at the start of the daily activities (eg., errands, travel, work), within 2 hours of waking, typically no later than
4 10:00am, and a calorie level between 20% and 35% of total daily energy needs 11. The Timlin definition is thus far the most comprehensive and inclusive definition proposed. Studies have identified central components of the breakfast meal that contribute to the association between breakfast and weight: macronutrient composition 6, 12, 13, caloric load, energy density and volume of the breakfast meal 14-16, and the time of day breakfast is consumed 17. The macronutrient component includes carbohydrate, protein, and fat; energy density is the measure of the energy contained in food quantified as calories per unit mass of food; and volume is the measure of the energy contained in food quantified as calories per unit volume of food. Studies to date have explored the physiologic satiety response of these components but not in the context of the breakfast meal. The aim of this review is to focus on the physiologic action that can help describe the relationship between breakfast and weight regulation. We identified the components of breakfast that have been shown in descriptive studies to have the greatest influence in the breakfast weight relationship. Further, we described the possible physiologic mechanisms linking these key components of breakfast to weight regulation. Finally we reviewed the few random controlled trials that have evaluated the physiologic difference between breakfast eating and breakfast skipping. Our goal is to clarify the most influential components of the breakfast-weight relationship through established physiologic action.
Assessment of breakfast and weight The relationship between breakfast and weight has been shown in children and adolescents as well as in adults 5, 7, 9, 12, 18-24. Table 1 is a comprehensive (but not complete) list of studies that
5 have evaluated the relationship between breakfast consumption and body weight and/or total daily energy intake in cross sectional, longitudinal, and/or as cross over investigations. The studies listed in table 1 evaluated breakfast pattern in general but did not identify specific characteristics of the breakfast meal. These studies provide insight about the relationship between breakfast and weight regulation. However, there are several influential components of the breakfast meal that can help explain its influence on food intake and weight regulation. Influential components of breakfast Breakfast macronutrient composition
The analysis of dietary composition and weight has
provided evidence that not all breakfast foods are created equal in terms of their effect on weight control. Table 2 provides a list of studies that have looked specifically at the macronutrient profile of breakfast in relation to subjective feelings of satiety, total daily calorie intake, and/or body weight and BMI. Collectively these data suggests that breakfast type is a significant factor for weight regulation. Most notably, cereal grains (often as ready to eat cereal) have been associated with a healthy weight more often than any other breakfast type 6, 13, 25-30. Any edible seed produced from the grass family is considered a cereal grain; examples include: barely, corn, oats, rice, wheat, and rye. Further, consumption of whole cereal grains provide more fiber compared to a low fiber alternative which leads to higher subjective satiety and a lower overall energy intake from breakfast 31-33. The satiating properties of breakfast meals high in protein, fat, or other carbohydrate sources have not been characterized to the same extent as cereal grains. However, a few studies have shown that a high protein breakfast compared to normal protein breakfast leads to higher initial and sustained feelings of fullness 34, 35. Also, when a high protein breakfast was compared to a
6 high carbohydrate breakfast, the high protein breakfast suppressed hunger better over a 24 hour period 36. In contrast to cereal grains and protein, a high fat breakfast has been predominately related to a poor ability to suppress hunger and is associated with higher total daily energy intake 37-39. It should be noted that, people who regularly consume low fat breakfasts have lower dietary fat intake overall and are more likely to have a lower body weight 7, 40. Therefore a breakfast low in dietary fat seems to be an important benefit for weight regulation. The data thus far show that cereal grains and protein rich breakfasts compared to breakfasts high in dietary fat promote higher subjective satiety and may help control total energy intake throughout the day. Caloric load, energy density or volume Another important component of breakfast is the amount of calories consumed during the breakfast meal. In two separate cross sectional analyses by de Castro et al. calorie consumption at breakfast was related to lower overall daily caloric intake 15, 17. The association of calories consumed at breakfast and weight gain was also shown to be inversely correlated when evaluated over time in middle aged men and women 16. But, as noted by Schusdziarra et al., previous studies have not consistently measured either absolute or relative breakfast calories and the influence of the ratio of breakfast to overall energy intake largely depends on post-breakfast intake rather than breakfast intake 41. Therefore, a clear interpretation of the effect of breakfast calorie load and total daily energy intake is still needed. Energy density is also an important factor in weight regulation. Energy density is measured as calories per unit weight of food; therefore food items that are high in fat are inherently more energy dense, as dietary fat provides twice as much energy per gram as carbohydrates or protein.
7 Studies have shown that energy density is associated with higher calorie consumption, but many of these studies could not eliminate the role of dietary fat as a consequence of elevated caloric intake 42, 43. In order to test the effect of energy density independent of macronutrient content Bell et al., developed three conditions of energy density by manipulating main entrées (breakfast, lunch, dinner) to create meals that had high (1800 ± 86kcal), medium (1519 ± 67), or low (1376 ± 43) energy density. The three energy density conditions were tested in a group of normal weight women. Their findings confirmed that the total amount of food consumed (by weight) was not different; therefore calorie intake was higher after the high density test day compared to the medium and low density test days 44. This finding is important because fat content was not responsible for the higher calorie intake; it was energy density specifically that led to higher calorie consumption. Energy density is distinctly connected to volume or calories per unit volume. For example manipulating energy density by incorporating water into food adds weight without adding calories and intrinsically decreases the calories per unit volume of food. Rolls et al. have extensively studied the benefits of high volume foods and found that when a high volume preload was provided to participants, the amount of food consumed at a lunch buffet was significantly lower than when participants consumed an isocaloric low volume preload 45. Rolls et al. continued their work by evaluating the effect of volume on food intake, independent of density. This evaluation was accomplished by incorporating air into test foods. Again, they found that by adding air to increase the volume of a test milkshake subsequent intake at a lunch meal was significantly lower than when the lunch was preceded by a low volume test milkshake 46. There is some, yet contested, evidence to suggest an inverse relationship between calories
8 consumed as a preload and total daily energy intake. However, solid evidence has been established for the role of energy density as well as volume on weight regulation. Meal timing
Research shows that the amount of food consumed at each meal increases as the
days goes on, while the satisfaction rating of each meal decreases as the day goes on 47. Moreover, the proportion of food intake in the morning is negatively correlated with overall intake, whereas a higher proportion of intake in the evening is correlated to a larger energy overall daily intake 15, 17. Similar findings come from the prospective evaluation of meal timing and BMI. In a prospective analysis of girls with a starting age between 8-12, those who consumed a higher mean percentage of energy in the evening were more likely to have a higher BMI at age 12-18 years of age 48. These findings suggest that it may be advantageous to consume a large breakfast to total food calorie ratio in the morning when meal satisfaction is higher, than consume a large evening meal when satisfaction is lower; postponed food intake may promote overconsumption. Overall the association found between these key influential components of breakfast can be further explained by their physiologic action. An in depth understanding of metabolic and endocrine physiology will help elucidate the what, how, and why breakfast is important.
Physiology of the satiety response based on influential breakfast components The satiety hormone response consists of a series of events that occur in anticipation and in response to meal consumption. The synergistic relationship between the endocrine system and the nervous system mediate the physiologic satiety response as well as subjective feelings of hunger and fullness. In addition, the control of food intake is composed of both short term and
9 long term energy regulation molecules. Short term or acute satiety signals dictate the amount of food consumed by responding to the acute feeding situation, whereas long term satiety signals refer to hormones that are secreted in proportion to fat stores 49. Regulatory satiety hormones and peptides are secreted from the gastrointestinal tract, the pancreas, and adipose tissue, as well as in the CNS. A variety of satiety hormones interact independently and/or synergistically through the CNS to elicit feelings of satiation and satiety. On the other hand circulating levels of ghrelin, which stimulates hunger, rises with fasting and falls after a meal 50, 51. Energy balance is achieved by the appropriate physiologic interaction between the short term acute response to food intake, the long term evaluation of energy stores, and feelings of hunger, which stimulate meal initiation. The interwoven neuroendocrine satiety response is constantly reformed by external stimuli such as macronutrient content, caloric load, energy density, and volume, as well as the time of the day food is consumed. The following section first gives a general description of key satiety hormones involved in food intake and weight regulation. Then the key components of breakfast are discussed in terms of their satiety related physiology.
Overview of Satiety Hormones Insulin is secreted by pancreatic -cells in response to elevated plasma glucose. Peripherally acting insulin is essential for blood glucose regulation as well as glycogen, triglyceride, and protein synthesis. Insulin also plays an essential role in the CNS as a neuropeptide, to decrease energy intake and increase energy expenditure 52, 53. Little or no insulin is secreted from within the CNS and therefore central insulin action is dependent on transport across the blood brain barrier by a saturable transport mechanism 54, 55.
10 Leptin is an adipokine produced predominately by white adipose tissue. In humans circulating leptin is directly related to the total number of white adipose cells and therefore correlates better with body fatness compared to body mass 56. Increased levels of circulating leptin have been shown to decrease food intake and increase energy expenditure in order to regulate body weight, this has been shown in all species studied to date 57, 58. As with insulin, leptin binds to and inhibits orexigenic neuropeptide Y (NPY) and agouti related protein (AgRP) containing neurons in the arcuate nucleus (ARC) while stimulating anorexigenic melanocortin stimulating hormone (MSH) and cocaine and amphetamine regulated transcript (CART) containing neurons 59. Leptin’s ability to regulate postprandial satiety is further enhanced through the synergistic relationship with cholecystokinin (CCK) 60, 61. Glucagon-like peptide-1 (GLP-1) is an incretin hormone. Thus, GLP-1 assists in regulating plasma glucose by enhancing insulin secretion and decreasing glucagon secretion after a meal 62, 63
. In addition to glucose regulation, GLP-1 is important in the regulation of food intake. In
humans and in animal models infusion of GLP-1 at the start of a meal decreases feelings of hunger and increases subjective satiety scores, it also inhibits food intake 64, 65. The specific mechanism of action is currently under investigation, but recent reports in animal models show that intracellular protein kinase A – mitogen activated protein kinase (PKA-MAPK) GLP-1 receptor activation in the nucleus tractus solitarus (NTS) decreases food intake and weight 66, 67. GLP-1 secretion reaches a peak 30-60 min after the consumption of food 68, and there is a greater release after larger meals 69. Cholecystokinin (CCK) was the first centrally administered gut derived hormone to induce a dose dependent, decrease in food intake 70. CCK is a short term regulator of food intake, as its effects on feeding are thought to be important for meal termination 71. In addition to being an
11 important factor in short term energy regulation, the anorexic action of CCK contributes to long term energy regulation by working in synergy with leptin. The combination of CCK and leptin administration has a potentiating effect leading to a more substantial decrease in food intake and weight loss than when either hormone is administered alone 60. CCK is secreted in response to fat and protein in the duodenum, and its action in the CNS is mediated through binding to and activating receptors located on the afferent vegus nerve 70, 72, 73. Ghrelin was the first peripheral hormone shown to stimulate hunger and food intake. It is primarily secreted by enterochromaffin cells in the fundic region of the stomach 74. In normal weight healthy humans ghrelin levels increase in between meals or during a fast, and decrease proportionally with food consumption. Ghrelin acts in opposition to insulin, leptin, and short term satiety signals in the CNS, by binding to receptors on neurons in the hypothalamus activating the orexigenic NPY/AgRP pathway 75-77. In addition to initiating hunger and food intake, ghrelin may influence macronutrient metabolism. Central and peripheral administration of ghrelin (within physiologic range) shows that ghrelin enhances carbohydrate metabolism, reduces fat metabolism and energy expenditure 78, 79. To date the primary function of ghrelin is to initiate food intake as well as preferentially store energy as fat by increasing lipogenesis and decreasing lipid oxidation. Additional energy regulatory hormones and peptides that are not mentioned above are involved in food consumption and weight regulation. Various adipokines, peptide YY, pancreatic polypeptide, oxyntomodulin, and amylin all influence energy intake to various degrees, and are important mediators of subjective feelings of satiety 49. On the other hand, the endogenous cannabinoid system is responsible for feelings of hunger and fosters orexigenic food intake behavior 80, 81.
12 Satiety and hunger hormone response to key components of breakfast The effect of key breakfast components (the focus of this review) on subjective and physiologic satiety responses are typically measured by one of two methods. One method is to provide participants with a test preload and then quantify food consumed at a subsequent standardized meal. The preload can be composed of any variation of the breakfast component in question. Another method is to provide isoenergetic meals or entire diets differing only in the breakfast component in question. Then food intake and/or hormone response can be compared between meals or diets. Total calories consumed, satiety (the time interval between meals), satiation (the point at which the meal episode ends), and the hormone responses are all informative outcome measures. This section will focus on studies that used either of the above mentioned methods to evaluate key breakfast components or breakfast omission. The physiology of macronutrients on satiety and hunger hormones, specifically cereal grains and breakfasts rich in protein, are discussed here. Cereal grains (as ready to eat cereal) are a common food consumed at breakfast. Cereal foods in the US provide a variety of nutritional benefits, one of which is dietary fiber. Data from large cross sectional studies show that cereal grain consumption is positively correlated with a higher proportion of fiber intake compared to non cereal grain consumers 5, 25, 26, 82. Cereal grains are rich in both soluble and insoluble fiber. In particular soluble fiber has the ability to influence satiety though bulking properties, viscosity, water holding capacity, and fermentation within the gastrointestinal tract 83. Pereira et al. provides a figure that shows physiologic pathways in which fiber can effect weight regulation. Studies show that the post prandial insulin response is improved when a high fiber breakfast is consumed 84. As depicted in the left path of figure 1, soluble fiber contained in a meal increases luminal viscosity which leads to decreased gastric emptying and hence a lower rate of glucose
13 uptake and subsequently lower insulin secretion 83. Further, bacterial fermentation of fibers resistant to enzymatic digestion produce short chain fatty acids in the lower gastrointestinal tract 85, 86
. Short chain fatty acids (acetate, butyrate, and propionate) appear to play a beneficial role
in glucose homeostasis, and stimulate the secretion of GLP-1 87-89. In addition the bulking properties of fiber rich meals promote a sustained increase in postprandial CCK 90, 91. Although other characteristics of cereal grains may contribute to weight regulation, fiber plays a key role as evidenced by its bulking properties and hence its stimulation of the satiety hormones insulin, GLP-1, and CCK all of which promote satiety. The majority of research findings have suggested that protein is the most satiating macronutrient 92-94
. Also, protein at breakfast has been shown to influence subsequent satiety hormone
regulation. When a high protein diet was compared to an adequate protein diet during weight loss, the satiety ratings during the high protein diet were associated with lower ghrelin and higher GLP-1 compared to a lower protein diet 95. Also, in an acute evaluation of 7-11 year old normal weight and obese children, the effect of a high protein breakfast was associated to a steady decline in ghrelin and steady increase in PYY, whereas the high carbohydrate and high fat breakfast equivalents elicited a less favorable ghrelin and PYY response 96. Dietary protein also stimulates the secretion of CCK 97. Thus, the associative finding that a breakfast rich in protein leads to increased satiety and decreased food intake is supported by controlled evaluations showing that protein consumption enhances stimulation of GLP-1, PYY, and CCK, also ghrelin is suppressed further contributing to the short term acute satiety response. In contrast to the beneficial effects of cereal grains and protein at breakfast, a high fat breakfast may lead to a decreased ability to control food intake. Studies in mice have shown that insulin resistance occurs during chronically high fat feeding 98. In another study of rats fed a high fat
14 (lard) diet the movement of insulin through the blood brain barrier was decreased, which is speculated to account for decreased satiation compared to regular chow fed rats 99. Still, diets high in fat have been shown to stimulate GLP-1 as well as CCK secretion in humans 100. Compared to participants following a low fat diet hunger ratings for participants following a chronic high fat diet were not affected by a high GLP-1 level during intraduadenal lipid infusion, 101
. This finding shows that despite elevated levels of GLP-1, a high fat dietary intake blunts the
effectiveness of the normal satiety response. Likewise, high fat meals do not increase circulating leptin to the same extent as a high carbohydrate meal in obese and normal weight women 102-104. Furthermore, ghrelin is not suppressed in response to a high fat meal to the same extent as an energy-matched high carbohydrate meal in men and women 105-107. The physiologic response to chronic high fat consumption promotes excessive intake of calories by overriding the appropriate satiety hormone response. These studies suggest that the macronutrient component of the breakfast meal is a key aspect in the association between breakfast consumption habits and weight regulation. Specifically breakfasts that are composed primarily of cereal grains and lean protein sources have a more advantageous association with food regulation compared to high fat breakfast foods. The physiology of caloric load, energy density and volume influences the satiety response and hence weight regulation. The caloric load of a meal is positively related to the secretion of GLP1, an essential incretin hormone. The relationship between caloric load and the incretin response is expected since circulating glucose increases with meal size, and GLP-1 activity is predominately under the influence of circulating glucose 108. A high calorie breakfast compared to a low calorie breakfast is positively correlated to GLP-1 and c-peptide (a surrogate marker for
15 insulin) 69. Caloric load was also shown to suppress ghrelin when participants were provided a liquid meal that varied in calorie load and/or volume 109. In addition to caloric load, energy density, and volume have a strong influence on satiety 110. This was confirmed in an experiment by Rolls et al. where participants were provided milk based drinks that varied only by volume. They found that when participants consumed the high volume drinks their subsequent food intake for the remainder of the day was decreased compared to when a low volume drink was consumed 45. The physiologic effect of high volume low energy dense foods can be explained by the action of both GLP-1 and CCK. Both hormones are secreted in response to a high volume food in the stomach and function to control the influx of nutrients from the stomach to the duodenum. These hormones mediate the delay in gastric emptying through regulation of pyloric sphincter pressure, stomach motility, and stomach muscle relaxation. As a consequence of GLP-1 and CCK’s ability to delay gastric emptying in the postprandial condition, stomach contents continue to apply pressure against the gastric wall, this pressure stimulates the firing rate of stretch afferent neurons, prolonging the feelings of satiety and satiation 111-113. In contrast, high energy dense low volume foods promote over consumption of calories. Energy dense food items are typically rich in fat and sugar and are highly palatable. The properties of palatability activate reward centers in the CNS, overriding systems that control food intake, and thereby dampen the action of satiety signaling 114. Overall studies show that caloric load may influence food intake through stimulation of GLP-1 and insulin as well as by suppressing ghrelin. Further, low energy dense and/or high volume foods influence food regulation though their physical action in the stomach as well as by
16 stimulating GLP-1 and CCK, mediating the delay in gastric emptying thereby enhancing stomach volume. The physiology of meal timing is best described for the long term satiety hormones insulin and leptin. Both hormones have been associated with a 24 hour circadian rhythm, and their pattern of secretion may also be further modified by meal timing. Insulin is tightly linked with meal timing, as glucose rises rapidly in response to meal consumption 115. In order to control for confounding influences on plasma glucose and insulin, researchers utilized a hyperglycemic clamp to evaluate insulin sensitivity over a 72 hr period. They found that insulin sensitivity follows a 24 hour circadian pattern; it is highest during the day and lowest at night 116. This finding may support studies that show lower insulin sensitivity in breakfast skippers 117. Similar to insulin, leptin is also influenced by diurnal rhythm. After evaluating leptin rhythm by 24 hour light/dark cycles, sleep/wake cycles, and meal timing researchers concluded that meal timing is the primary mediator of leptin rhythm. Their conclusion was formed from the fact that a 6.5 hour shift in meal timing acutely influenced leptin levels within hours of changing meal timing, but cortisol (which strongly correlates to 24 hr rhythm) did not change, suggesting that the 24 hour circadian entrainment of leptin is secondary to that of meal timing 118. Likewise, ghrelin is predominantly influenced by meal timing, as evidenced by circulating ghrelin at its highest level during fasting conditions and lowest level following food consumption. Elevated levels of circulating ghrelin are strongly correlated to feelings of hunger, thus the rise in circulating ghrelin is proposed to stimulate meal initiation 50, 51. This review illustrates how meal timing may play an important role in the regulation of physiologic satiety signals. So far only insulin and leptin, as well as the hunger hormone ghrelin,
17 have been implicated in this relationship, but it is certainly possible that short term satiety signals are influenced by the time of day a meal is consumed.
The physiology of skipping breakfast The physiologic consequence of skipping breakfast can be described in part by evaluating the consequence of short term fasting studies. Fasting conditions promote elevated levels of circulating free fatty acids (FFA), which have been shown to affect the binding ability of insulin to its receptor, creating a state of insulin insensitivity 119, 120. Breakfast omission is metabolically analogous to a short term fast, so FFA’s are elevated; this mechanism may explain the finding by Farshchi et al. that skipping breakfast is associated with decreased postprandial insulin sensitivity following a 14 day breakfast or no breakfast crossover intervention 117. Carlson et al. further evaluated breakfast skipping by providing participants with their daily calorie needs in three typically spaced meal times or as one large meal. This study found that when participants were provided one meal per day (consumed between 4pm and 8pm, for 8 weeks) their morning fasting plasma glucose was elevated and the response to an oral glucose tolerance test showed that there was a greater and more sustained plasma glucose and delayed insulin response compared to participants who consumed three meals per day 121. In another clinical evaluation of breakfast, Astbury et al. provided breakfast or no breakfast, followed by a pre load, and then an ad libitum lunch in a cross over designed study. In the no breakfast condition, glucose and insulin responses were higher; in the breakfast condition, GLP-1 and Peptide Y were higher in response to the preload 122. Leidy et al. evaluated the impact of a high protein breakfast, normal protein breakfast, or skipping breakfast on food intake and appetite in a group of typically
18 breakfast skipping adolescence. The response to the breakfast meals or skipping breakfast was evaluated over a 5 hour period. The results show that circulating PYY was lower following the skipping breakfast protocol compared to either breakfast 34. As discussed previously, plasma leptin is lower under acute fasting conditions compared to fed conditions; also, circulating leptin decreases as a result of prolonged energy restriction independent of adiposity 123. These periods of acute fasting and energy restriction produce a cumulative negative energy imbalance, and only by returning energy stores to cumulative energy balance will leptin increase back to steady state levels, proportional to adiposity 124. Thus skipping breakfast leads to longer periods of elevated ghrelin and lower levels of GLP-1 and peptide Y. This imbalance of satiety hormone physiology promotes hunger and leads to overconsumption (beyond energy balance) after periods of fasting. These few, but seminal, studies have identified that breakfast omission does influence the physiology of the satiety response. The long term regulators of energy intake insulin and leptin are modified during periods of fasting and energy imbalance. In addition, skipping breakfast negatively impacts the acute physiologic response of PYY and ghrelin.
Linking the breakfast weight relationship: confounding factors Although substantial evidence supports the role of breakfast on weight regulation, not all investigations have come to the same conclusion. Table 3 provides a list of non significant associations between breakfast and food intake regulation and/or weight. The incongruent findings in table 3 are a result of the non significant main effect between breakfast and weight/BMI or food intake, or a no longer significant association when potential confounding factors were accounted for 10, 125-128.
19 Differences in methodology contribute to the contradictory results seen in breakfast literature. Dialektakou et al. examined the interaction of breakfast skipping with both body weight as well as BMI-overweight/obesity; in addition, breakfast habits were compared using unadjusted results and results adjusted for potential confounders; further, breakfast habits were compared with 24 different definitions of breakfast skipping. The assessment of various measures of body fatness, potential confounding factors, and breakfast definitions showed that fewer breakfast skipping variables were associated with BMI than with overweight/obesity, fewer associations were found when controlling for than when not controlling for potential confounders, and fewer associations were found for variables corresponding to some definitions of breakfast skipping than for variables corresponding to other definitions of breakfast 129. Health professionals are and will continue to be limited in their ability to advise about what, how much, and when to eat breakfast if research on breakfast does not conform to a standard definition and the various components of breakfast are not controlled for. As mentioned previously the definition for breakfast stated by Timlin et. al. would serve well as the standard in further research.
Conclusion and direction of future research The aim of this review was to provide evidence for and discus the physiologic mechanisms that mediate the association between breakfast consumption and weight regulation. The main findings were that meal macronutrient composition specifically cereal grains and protein rich breakfasts promote higher subjective satiety and may help control total daily energy intake. Cereal grains may further contribute to weight regulation by providing soluble fiber which physically and metabolically influences the action of satiety hormones insulin, GLP-1, and CCK,
20 all of which promote satiety. In addition, a protein rich breakfast may enhance the satiety response of GLP-1, CCK, and PYY which support feelings of fullness and are associated with decreased food intake. Caloric load, density, and volume of the breakfast meal increase feelings of satiety thereby playing an important role in weight regulation. GLP-1 and insulin are secreted in proportion to caloric load while the opposite is true for the hunger hormone ghrelin. Low energy dense and/or high volume foods influence satiety though their physical action in the stomach by stimulating GLP-1 and CCK response. Meal timing is an important factor in insulin and leptin rhythms of secretion. In addition the hunger hormone ghrelin is primarily entrained by the timing of meal consumption. With the evidence presented here, we conclude that breakfast skipping has a detrimental impact on the physiology of the satiety response. The physiology discussed throughout this review could be applied to lunch and dinner as well as breakfast. However, the breakfast meal seems to be especially influential in weight regulation. The benefit of breakfast is likely a consequence of the prolonged physiologic state which is supportive of satiety and depressive toward feelings of hunger. When breakfast is consumed this physiologic satiety state can be beneficial for the entire day as opposed to the physiology of the satiety hormone response when food intake is postponed till later in the day. The course of future research should first be to implement a standard definition for breakfast. In addition, further investigation is needed to clarify the optimal time of day breakfast should be consumed and how to incorporate the most advantageous breakfast composition, density, and volume into a public health recommendation.
21 Bibliography 1
Kant AK, Graubard BI. Secular trends in patterns of self-reported food consumption of adult Americans: NHANES 1971-1975 to NHANES 1999-2002. Am J Clin Nutr: United States 2006; 1215-23.
2
Flegal KM, Carroll MD, Ogden CL, Johnson CL. Prevalence and trends in obesity among US adults, 1999-2000. JAMA. 2002; 288: 1723-7.
3
Hedley AA, Ogden CL, Johnson CL, Carroll MD, Curtin LR, Flegal KM. Prevalence of overweight and obesity among US children, adolescents, and adults, 1999-2002. JAMA. 2004; 291: 2847-50.
4
Rampersaud GC, Pereira MA, Girard BL, Adams J, Metzl JD. Breakfast habits, nutritional status, body weight, and academic performance in children and adolescents. J Am Diet Assoc. 2005; 105: 743-60; quiz 61-2.
5
Affenito SG, Thompson DR, Barton BA, Franko DL, Daniels SR, Obarzanek E, et al. Breakfast consumption by African-American and white adolescent girls correlates positively with calcium and fiber intake and negatively with body mass index. J Am Diet Assoc: United States 2005; 938-45.
6
Song WO, Chun OK, Obayashi S, Cho S, Chung CE. Is Consumption of Breakfast Associated with Body Mass Index in US Adults? Journal of the American Dietetic Association. 2005; 105: 1373-82.
7
Timlin MT, Pereira MA, Story M, Neumark-Sztainer D. Breakfast eating and weight change in a 5-year prospective analysis of adolescents: Project EAT (Eating Among Teens). Pediatrics. 2008; 121: e638-45.
8
Keski-Rahkonen A, Kaprio J, Rissanen A, Virkkunen M, Rose RJ. Breakfast skipping and health-compromising behaviors in adolescents and adults. Eur J Clin Nutr. 2003; 57: 842-53.
9
Ortega RM, Requejo AM, Lopez-Sobaler AM, Quintas ME, Andres P, Redondo MR, et al. Difference in the breakfast habits of overweight/obese and normal weight schoolchildren. Int J Vitam Nutr Res. 1998; 68: 125-32.
10
Williams P. Breakfast and the diets of Australian adults: an analysis of data from the 1995 National Nutrition Survey. Int J Food Sci Nutr. 2005; 56: 65-79.
22 11
Timlin M, Pereira M. Breakfast Frequency and Quality in the Etiology of Adult Obesity and Chronic Diseases. Nutrition Reviews. 2008; Volume 65: 268-81.
12
Wyatt HR, Grunwald GK, Mosca CL, Klem ML, Wing RR, Hill JO. Long-term weight loss and breakfast in subjects in the National Weight Control Registry. Obes Res. 2002; 10: 78-82.
13
Cho S, Dietrich M, Brown CJ, Clark CA, Block G. The effect of breakfast type on total daily energy intake and body mass index: results from the Third National Health and Nutrition Examination Survey (NHANES III). J Am Coll Nutr. 2003; 22: 296-302.
14
Martin A, Normand S, Sothier M, Peyrat J, Louche-Pelissier C, Laville M. Is advice for breakfast consumption justified? Results from a short-term dietary and metabolic experiment in young healthy men. Br J Nutr. 2000; 84: 337-44.
15
De Castro JM. When, how much and what foods are eaten are related to total daily food intake. British Journal of Nutrition. 2009; 102: 1228-37.
16
Purslow LR, Sandhu MS, Forouhi N, Young EH, Luben RN, Welch AA, et al. Energy intake at breakfast and weight change: Prospective study of 6,764 middle-aged men and women. American Journal of Epidemiology. 2008; 167: 188-92.
17
De Castro JM. The time of day of food intake influences overall intake in humans. J Nutr. 2004; 134: 104-11.
18
Alexander KE, Ventura EE, Spruijt-Metz D, Weigensberg MJ, Goran MI, Davis JN. Association of breakfast skipping with visceral fat and insulin indices in overweight Latino youth. Obesity (Silver Spring): United States 2009; 1528-33.
19
Berkey CS, Rockett HR, Gillman MW, Field AE, Colditz GA. Longitudinal study of skipping breakfast and weight change in adolescents. Int J Obes Relat Metab Disord. 2003; 27: 1258-66.
20
Dubois L, Girard M, Potvin Kent M, Farmer A, Tatone-Tokuda F. Breakfast skipping is associated with differences in meal patterns, macronutrient intakes and overweight among pre-school children. Public Health Nutr: England 2009; 19-28.
21
Elfhag K, Rossner S. Who succeeds in maintaining weight loss? A conceptual review of factors associated with weight loss maintenance and weight regain. Obes Rev. 2005; 6: 67-85.
23 22
Ma Y, Bertone ER, Stanek EJ, 3rd, Reed GW, Hebert JR, Cohen NL, et al. Association between eating patterns and obesity in a free-living US adult population. Am J Epidemiol. 2003; 158: 85-92.
23
Szajewska H, Ruszczynski M. Systematic review demonstrating that breakfast consumption influences body weight outcomes in children and adolescents in Europe. Crit Rev Food Sci Nutr: England 2010; 113-9.
24
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). 2007;15: 2463-9.
25
Albertson AM, Anderson GH, Crockett SJ, Goebel MT. Ready-to-eat cereal consumption: its relationship with BMI and nutrient intake of children aged 4 to 12 years. J Am Diet Assoc. 2003; 103: 1613-9.
26
Albertson AM, Thompson D, Franko DL, Holschuh NM, Bauserman R, Barton BA. Prospective Associations among Cereal Intake in Childhood and Adiposity, Lipid Levels, and Physical Activity during Late Adolescence. Journal of the American Dietetic Association. 2009; 109: 1775-80.
27
Barton BA, Eldridge AL, Thompson D, Affenito SG, Striegel-Moore RH, Franko DL, et al. The relationship of breakfast and cereal consumption to nutrient intake and body mass index: the National Heart, Lung, and Blood Institute Growth and Health Study. J Am Diet Assoc: United States 2005; 1383-9.
28
Bazzano LA, Song Y, Bubes V, Good CK, Manson JE, Liu S. Dietary intake of whole and refined grain breakfast cereals and weight gain in men. Obes Res: United States 2005; 1952-60.
29
Deshmukh-Taskar PR, Nicklas TA, O'Neil CE, Keast DR, Radcliffe JD, Cho S. The relationship of breakfast skipping and type of breakfast consumption with nutrient intake and weight status in children and adolescents: the National Health and Nutrition Examination Survey 1999-2006. J Am Diet Assoc. 2010 American Dietetic Association. Published by Elsevier Inc: United States 2010; 869-78.
30
Williams BM, O'Neil CE, Keast DR, Cho S, Nicklas TA. Are breakfast consumption patterns associated with weight status and nutrient adequacy in African-American children? Public Health Nutr. 2009; 12: 489-96.
24 31
Hamedani A, Akhavan T, Samra RA, Anderson GH. Reduced energy intake at breakfast is not compensated for at lunch if a high-insoluble-fiber cereal replaces a low-fiber cereal. Am J Clin Nutr. 2009; 89: 1343-9.
32
Holt SH, Delargy HJ, Lawton CL, Blundell JE. The effects of high-carbohydrate vs highfat breakfasts on feelings of fullness and alertness, and subsequent food intake. Int J Food Sci Nutr. 1999; 50: 13-28.
33
Burley VJ, Leeds AR, Blundell JE. The effect of high and low-fibre breakfasts on hunger, satiety and food intake in a subsequent meal. Int J Obes. 1987; 11 Suppl 1: 87-93.
34
Leidy H, Bossingham M, Mattes R, Campbell W. Increased dietary protein consumed at breakfast leads to an initial and sustained feeling of fullness during energy restriction compared to other meal times. Br J Nutr. 2009; 101: 798-803.
35
Leidy HJ, Racki EM. The addition of a protein-rich breakfast and its effects on acute appetite control and food intake in 'breakfast-skipping' adolescents. International Journal of Obesity. 2010; 34: 1125-33.
36
Stubbs RJ, van Wyk MC, Johnstone AM, Harbron CG. Breakfasts high in protein, fat or carbohydrate: effect on within-day appetite and energy balance. Eur J Clin Nutr. 1996; 50: 409-17.
37
Clegg M, Shafat A. Energy and macronutrient composition of breakfast affect gastric emptying of lunch and subsequent food intake, satiety and satiation. Appetite. 2010; 54: 517-23.
38
Cotton JR, Burley VJ, Weststrate JA, Blundell JE. Dietary fat and appetite: similarities and differences in the satiating effect of meals supplemented with either fat or carbohydrate. J Hum Nutr Diet. 2007; 20: 186-99.
39
Blundell JE, Burley VJ, Cotton JR, Lawton CL. Dietary fat and the control of energy intake: evaluating the effects of fat on meal size and postmeal satiety. Am J Clin Nutr. 1993; 57: 772S-77S; discussion 77S-78S.
40
Morgan KJ, Zabik ME, Stampley GL. The role of breakfast in diet adequacy of the U.S. adult population. J Am Coll Nutr. 1986; 5: 551-63.
41
Schusdziarra V, Hausmann M, Wittke C, Mittermeier J, Kellner M, Naumann A, et al. Impact of breakfast on daily energy intake--an analysis of absolute versus relative breakfast calories. Nutr J. 2011; 10: 5.
25 42
Duncan KH, Bacon JA, Weinsier RL. The effects of high and low energy density diets on satiety, energy intake, and eating time of obese and nonobese subjects. Am J Clin Nutr. 1983; 37: 763-7.
43
Stubbs RJ, Johnstone AM, O'Reilly LM, Barton K, Reid C. The effect of covertly manipulating the energy density of mixed diets on ad libitum food intake in 'pseudo freeliving' humans. Int J Obes Relat Metab Disord. 1998; 22: 980-7.
44
Bell EA, Castellanos VH, Pelkman CL, Thorwart ML, Rolls BJ. Energy density of foods affects energy intake in normal-weight women. Am J Clin Nutr. 1998; 67: 412-20.
45
Rolls BJ, Castellanos VH, Halford JC, Kilara A, Panyam D, Pelkman CL, et al. Volume of food consumed affects satiety in men. Am J Clin Nutr. 1998; 67: 1170-7.
46
Rolls BJ, Bell EA, Waugh BA. Increasing the volume of a food by incorporating air affects satiety in men. Am J Clin Nutr. 2000; 72: 361-8.
47
De Castro JM. Circadian rhythms of the spontaneous meal pattern, macronutrient intake, and mood of humans. Physiol Behav. 1987; 40: 437-46.
48
Thompson OM, Ballew C, Resnicow K, Gillespie C, Must A, Bandini LG, et al. Dietary pattern as a predictor of change in BMI z-score among girls. Int J Obes (Lond). 2006; 30: 176-82.
49
Schwartz MW, Woods SC, Porte D, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature. 2000; 404: 661-71.
50
Cummings DE, Purnell JQ, Frayo RS, Schmidova K, Wisse BE, Weigle DS. A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes. 2001; 50: 1714-9.
51
Cummings DE, Frayo RS, Marmonier C, Aubert R, Chapelot D. Plasma ghrelin levels and hunger scores in humans initiating meals voluntarily without time- and food-related cues. Am J Physiol Endocrinol Metab. 2004; 287: E297-304.
52
Holt SH, Brand Miller JC, Petocz P. Interrelationships among postprandial satiety, glucose and insulin responses and changes in subsequent food intake. Eur J Clin Nutr. 1996; 50: 788-97.
53
Stockhorst U, de Fries D, Steingrueber HJ, Scherbaum WA. Insulin and the CNS: effects on food intake, memory, and endocrine parameters and the role of intranasal insulin administration in humans. Physiol Behav. 2004; 83: 47-54.
26 54
Baura GD, Foster DM, Porte D, Jr., Kahn SE, Bergman RN, Cobelli C, et al. Saturable transport of insulin from plasma into the central nervous system of dogs in vivo. A mechanism for regulated insulin delivery to the brain. J Clin Invest. 1993; 92: 1824-30.
55
Banks WA. The source of cerebral insulin. Eur J Pharmacol. 2004; 490: 5-12.
56
Considine RV, Caro JF. Leptin in humans: current progress and future directions. Clin Chem. 1996; 42: 843-4.
57
Tang-Christensen M, Havel PJ, Jacobs RR, Larsen PJ, Cameron JL. Central administration of leptin inhibits food intake and activates the sympathetic nervous system in rhesus macaques. J Clin Endocrinol Metab. 1999; 84: 711-7.
58
Tang-Christensen M, Larsen PJ, Thulesen J, Rømer J, Vrang N. The proglucagon-derived peptide, glucagon-like peptide-2, is a neurotransmitter involved in the regulation of food intake. Nat Med. 2000; 6: 802-7.
59
Cowley MA, Smart JL, Rubinstein M, Cerdán MG, Diano S, Horvath TL, et al. Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature. 2001; 411: 480-4.
60
Matson CA, Wiater MF, Kuijper JL, Weigle DS. Synergy between leptin and cholecystokinin (CCK) to control daily caloric intake. Peptides. 1997; 18: 1275-8.
61
Matson CA, Reid DF, Cannon TA, Ritter RC. Cholecystokinin and leptin act synergistically to reduce body weight. Am J Physiol Regul Integr Comp Physiol. 2000; 278: R882-90.
62
Holst JJ. The physiology of glucagon-like peptide 1. Physiol Rev. 2007; 87: 1409-39.
63
Holst JJ, Christensen M, Lund A, de Heer J, Svendsen B, Kielgast U, et al. Regulation of glucagon secretion by incretins. Diabetes Obes Metab. 2011; 13 Suppl 1: 89-94.
64
Verdich C, Flint A, Gutzwiller JP, Naslund E, Beglinger C, Hellstrom PM, et al. A metaanalysis of the effect of glucagon-like peptide-1 (7-36) amide on ad libitum energy intake in humans. J Clin Endocrinol Metab. 2001; 86: 4382-9.
65
Gutzwiller JP, Degen L, Heuss L, Beglinger C. Glucagon-like peptide 1 (GLP-1) and eating. Physiol Behav. 2004; 82: 17-9.
66
Hayes MR, Bradley L, Grill HJ. Endogenous hindbrain glucagon-like peptide-1 receptor activation contributes to the control of food intake by mediating gastric satiation signaling. Endocrinology. 2009; 150: 2654-9.
27 67
Hayes MR, Leichner TM, Zhao S, Lee GS, Chowansky A, Zimmer D, et al. Intracellular signals mediating the food intake-suppressive effects of hindbrain glucagon-like peptide1 receptor activation. Cell Metab. 2011; 13: 320-30.
68
Lugari R, Dell'Anna C, Ugolotti D, Dei Cas A, Barilli AL, Zandomeneghi R, et al. Effect of nutrient ingestion on glucagon-like peptide 1 (7-36 amide) secretion in human type 1 and type 2 diabetes. Horm Metab Res. 2000; 32: 424-8.
69
Vilsbøll T, Krarup T, Sonne J, Madsbad S, Vølund A, Juul AG, et al. Incretin secretion in relation to meal size and body weight in healthy subjects and people with type 1 and type 2 diabetes mellitus. J Clin Endocrinol Metab. 2003; 88: 2706-13.
70
Gibbs J, Young RC, Smith GP. Cholecystokinin decreases food intake in rats. J Comp Physiol Psychol. 1973; 84: 488-95.
71
Moran TH. Cholecystokinin and satiety: current perspectives. Nutrition. 2000; 16: 85865.
72
Degen L, Matzinger D, Drewe J, Beglinger C. The effect of cholecystokinin in controlling appetite and food intake in humans. Peptides. 2001; 22: 1265-9.
73
Moran TH, Schwartz GJ. Neurobiology of cholecystokinin. Crit Rev Neurobiol. 1994; 9: 1-28.
74
Kojima M, Kangawa K. Ghrelin: from gene to physiological function. Results Probl Cell Differ. 2010; 50: 185-205.
75
Nakazato M, Murakami N, Date Y, Kojima M, Matsuo H, Kangawa K, et al. A role for ghrelin in the central regulation of feeding. Nature. 2001; 409: 194-8.
76
Shintani M, Ogawa Y, Ebihara K, Aizawa-Abe M, Miyanaga F, Takaya K, et al. Ghrelin, an endogenous growth hormone secretagogue, is a novel orexigenic peptide that antagonizes leptin action through the activation of hypothalamic neuropeptide Y/Y1 receptor pathway. Diabetes. 2001; 50: 227-32.
77
Chen HY, Trumbauer ME, Chen AS, Weingarth DT, Adams JR, Frazier EG, et al. Orexigenic action of peripheral ghrelin is mediated by neuropeptide Y and agouti-related protein. Endocrinology. 2004; 145: 2607-12.
78
Theander-Carrillo C, Wiedmer P, Cettour-Rose P, Nogueiras R, Perez-Tilve D, Pfluger P, et al. Ghrelin action in the brain controls adipocyte metabolism. J Clin Invest. 2006; 116: 1983-93.
28 79
Tsubone T, Masaki T, Katsuragi I, Tanaka K, Kakuma T, Yoshimatsu H. Ghrelin regulates adiposity in white adipose tissue and UCP1 mRNA expression in brown adipose tissue in mice. Regul Pept. 2005; 130: 97-103.
80
Engeli S. Central and peripheral cannabinoid receptors as therapeutic targets in the control of food intake and body weight. Handb Exp Pharmacol. 2012: 357-81.
81
Kirkham TC, Williams CM. Endogenous cannabinoids and appetite. Nutr Res Rev. 2001; 14: 65-86.
82
Albertson AM, Thompson D, Franko DL, Kleinman RE, Barton BA, Crockett SJ. Consumption of breakfast cereal is associated with positive health outcomes: evidence from the National Heart, Lung, and Blood Institute Growth and Health Study. Nutr Res. 2008; 28: 744-52.
83
Pereira MA, Ludwig DS. Dietary fiber and body-weight regulation. Observations and mechanisms. Pediatr Clin North Am. 2001; 48: 969-80.
84
Clark CA, Gardiner J, McBurney MI, Anderson S, Weatherspoon LJ, Henry DN, et al. Effects of breakfast meal composition on second meal metabolic responses in adults with Type 2 diabetes mellitus. Eur J Clin Nutr. Published online 3 May 2006.: England 2006; 1122-9.
85
Jenkins DJ, Wolever TM, Taylor RH, Griffiths C, Krzeminska K, Lawrie JA, et al. Slow release dietary carbohydrate improves second meal tolerance. Am J Clin Nutr. 1982; 35: 1339-46.
86
Wolever TM, Jenkins DJ, Ocana AM, Rao VA, Collier GR. Second-meal effect: lowglycemic-index foods eaten at dinner improve subsequent breakfast glycemic response. Am J Clin Nutr. 1988; 48: 1041-7.
87
Reimer RA, McBurney MI. Dietary fiber modulates intestinal proglucagon messenger ribonucleic acid and postprandial secretion of glucagon-like peptide-1 and insulin in rats. Endocrinology. 1996; 137: 3948-56.
88
Cani PD, Hoste S, Guiot Y, Delzenne NM. Dietary non-digestible carbohydrates promote L-cell differentiation in the proximal colon of rats. Br J Nutr. 2007; 98: 32-7.
89
Cani PD, Lecourt E, Dewulf EM, Sohet FM, Pachikian BD, Naslain D, et al. Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide
29 production with consequences for appetite sensation and glucose response after a meal. Am J Clin Nutr. 2009; 90: 1236-43. 90
Bourdon I, Olson B, Backus R, Richter BD, Davis PA, Schneeman BO. Beans, as a source of dietary fiber, increase cholecystokinin and apolipoprotein b48 response to test meals in men. J Nutr. 2001; 131: 1485-90.
91
Holt S, Brand J, Soveny C, Hansky J. Relationship of satiety to postprandial glycemic, insulin, and cholecystokinin responses. Appetite. 1992; 18: 129-41.
92
Johnstone AM, Stubbs RJ, Harbron CG. Effect of overfeeding macronutrients on day-today food intake in man. Eur J Clin Nutr. 1996; 50: 418-30.
93
De Castro JM. What are the major correlates of macronutrient selection in Western populations? Proc Nutr Soc. 1999; 58: 755-63.
94
Marmonier C, Chapelot D, Louis-Sylvestre J. Effects of macronutrient content and energy density of snacks consumed in a satiety state on the onset of the next meal. Appetite. 2000; 34: 161-8.
95
Lejeune MP, Westerterp KR, Adam TC, Luscombe-Marsh ND, Westerterp-Plantenga MS. Ghrelin and glucagon-like peptide 1 concentrations, 24-h satiety, and energy and substrate metabolism during a high-protein diet and measured in a respiration chamber. Am J Clin Nutr. 2006; 83: 89-94.
96
Lomenick JP, Melguizo MS, Mitchell SL, Summar ML, Anderson JW. Effects of meals high in carbohydrate, protein, and fat on ghrelin and peptide YY secretion in prepubertal children. J Clin Endocrinol Metab. 2009; 94: 4463-71.
97
Hopman WP, Jansen JB, Lamers CB. Comparative study of the effects of equal amounts of fat, protein, and starch on plasma cholecystokinin in man. Scand J Gastroenterol. 1985; 20: 843-7.
98
Kim JK, Gimeno RE, Higashimori T, Kim HJ, Choi H, Punreddy S, et al. Inactivation of fatty acid transport protein 1 prevents fat-induced insulin resistance in skeletal muscle. J Clin Invest. 2004; 113: 756-63.
99
Gerozissis K, Orosco M, Rouch C, Nicolaidis S. Insulin responses to a fat meal in hypothalamic microdialysates and plasma. Physiol Behav. 1997; 62: 767-72.
100
Baggio LL, Drucker DJ. Biology of incretins: GLP-1 and GIP. Gastroenterology. 2007; 132: 2131-57.
30 101
Boyd KA, O'Donovan DG, Doran S, Wishart J, Chapman IM, Horowitz M, et al. Highfat diet effects on gut motility, hormone, and appetite responses to duodenal lipid in healthy men. Am J Physiol Gastrointest Liver Physiol. 2003; 284: G188-96.
102
Romon M, Lebel P, Fruchart JC, Dallongeville J. Postprandial leptin response to carbohydrate and fat meals in obese women. J Am Coll Nutr. 2003; 22: 247-51.
103
Havel PJ, Townsend R, Chaump L, Teff K. High-fat meals reduce 24-h circulating leptin concentrations in women. Diabetes. 1999; 48: 334-41.
104
Havel PJ. Update on adipocyte hormones: regulation of energy balance and carbohydrate/lipid metabolism. Diabetes. 2004; 53 Suppl 1: S143-51.
105
Pavlatos S, Kokkinos A, Tentolouris N, Doupis J, Kyriaki D, Katsilambros N. Acute effects of high-protein and high-fat isoenergetic meals on total ghrelin plasma concentrations in lean and obese women. Horm Metab Res. 2005; 37: 773-5.
106
Foster-Schubert KE, McTiernan A, Frayo RS, Schwartz RS, Rajan KB, Yasui Y, et al. Human plasma ghrelin levels increase during a one-year exercise program. J Clin Endocrinol Metab. 2005; 90: 820-5.
107
Koliaki C, Kokkinos A, Tentolouris N, Katsilambros N. The effect of ingested macronutrients on postprandial ghrelin response: a critical review of existing literature data. Int J Pept. 2010; 2010.
108
Kreymann B, Williams G, Ghatei MA, Bloom SR. Glucagon-like peptide-1 7-36: a physiological incretin in man. Lancet. 1987; 2: 1300-4.
109
le Roux CW, Patterson M, Vincent RP, Hunt C, Ghatei MA, Bloom SR. Postprandial plasma ghrelin is suppressed proportional to meal calorie content in normal-weight but not obese subjects. J Clin Endocrinol Metab. 2005; 90: 1068-71.
110
Poppitt SD, Prentice AM. Energy density and its role in the control of food intake: evidence from metabolic and community studies. Appetite. 1996; 26: 153-74.
111
Flint A, Raben A, Ersbøll AK, Holst JJ, Astrup A. The effect of physiological levels of glucagon-like peptide-1 on appetite, gastric emptying, energy and substrate metabolism in obesity. Int J Obes Relat Metab Disord. 2001; 25: 781-92.
112
Melton PM, Kissileff HR, Pi-Sunyer FX. Cholecystokinin (CCK-8) affects gastric pressure and ratings of hunger and fullness in women. Am J Physiol. 1992; 263: R452-6.
31 113
Kissileff HR, Carretta JC, Geliebter A, Pi-Sunyer FX. Cholecystokinin and stomach distension combine to reduce food intake in humans. Am J Physiol Regul Integr Comp Physiol. 2003; 285: R992-8.
114
Erlanson-Albertsson C. How palatable food disrupts appetite regulation. Basic Clin Pharmacol Toxicol. 2005; 97: 61-73.
115
Polonsky KS, Given BD, Van Cauter E. Twenty-four-hour profiles and pulsatile patterns of insulin secretion in normal and obese subjects. J Clin Invest. 1988; 81: 442-8.
116
Boden G, Chen X, Urbain JL. Evidence for a circadian rhythm of insulin sensitivity in patients with NIDDM caused by cyclic changes in hepatic glucose production. Diabetes. 1996; 45: 1044-50.
117
Farshchi HR, Taylor MA, Macdonald IA. Deleterious effects of omitting breakfast on insulin sensitivity and fasting lipid profiles in healthy lean women. Am J Clin Nutr. 2005; 81: 388-96.
118
Schoeller DA, Cella LK, Sinha MK, Caro JF. Entrainment of the diurnal rhythm of plasma leptin to meal timing. J Clin Invest. 1997; 100: 1882-7.
119
Belfort R, Mandarino L, Kashyap S, Wirfel K, Pratipanawatr T, Berria R, et al. Doseresponse effect of elevated plasma free fatty acid on insulin signaling. Diabetes. 2005; 54: 1640-8.
120
Kruszynska YT, Mulford MI, Yu JG, Armstrong DA, Olefsky JM. Effects of nonesterified fatty acids on glucose metabolism after glucose ingestion. Diabetes. 1997; 46: 1586-93.
121
Carlson O, Martin B, Stote KS, Golden E, Maudsley S, Najjar SS, et al. Impact of reduced meal frequency without caloric restriction on glucose regulation in healthy, normal-weight middle-aged men and women. Metabolism. 2007; 56: 1729-34.
122
Astbury NM, Taylor MA, Macdonald IA. Breakfast Consumption Affects Appetite, Energy Intake, and the Metabolic and Endocrine Responses to Foods Consumed Later in the Day in Male Habitual Breakfast Eaters. Journal of Nutrition. 2011; 141: 1381-89.
123
Keim NL, Stern JS, Havel PJ. Relation between circulating leptin concentrations and appetite during a prolonged, moderate energy deficit in women. Am J Clin Nutr. 1998; 68: 794-801.
32 124
Chin-Chance C, Polonsky KS, Schoeller DA. Twenty-four-hour leptin levels respond to cumulative short-term energy imbalance and predict subsequent intake. J Clin Endocrinol Metab. 2000; 85: 2685-91.
125
Sampson AE, Dixit S, Meyers AF, Houser R, Jr. The nutritional impact of breakfast consumption on the diets of inner-city African-American elementary school children. J Natl Med Assoc. 1995; 87: 195-202.
126
Berteus Forslund H, Lindroos AK, Sjostrom L, Lissner L. Meal patterns and obesity in Swedish women-a simple instrument describing usual meal types, frequency and temporal distribution. Eur J Clin Nutr. 2002; 56: 740-7.
127
Williams P. Breakfast and the diets of Australian children and adolescents: an analysis of data from the 1995 National Nutrition Survey. Int J Food Sci Nutr. 2007; 58: 201-16.
128
Fujiwara T, Nakata R. Skipping breakfast is associated with reproductive dysfunction in post-adolescent female college students. Appetite. 2010; 55: 714-7.
129
Dialektakou KD, Vranas PB. Breakfast skipping and body mass index among adolescents in Greece: whether an association exists depends on how breakfast skipping is defined.. J Am Diet Assoc. 2008; 108:
33
33
Table 1
Appendix 1
Author
Studies assessing the relationship between breakfast and body weight and/or total daily energy intake Research Design
participants
Breakfast Definition
2,397 girls
Any eating that occurred between 5 am and 10 am weekdays or between 5 am and 11 am during weekends
65 boys and 45 girls
Any food or beverage consumed between 5am and 10am and ≥ 100kcal during two 24 hr recalls
Affenito et al. 2005
Nutrient intake and BMI. 9 yr Prospective National Heart, Lung, and Blood Institute Growth and Health Study
Alexander et al. 2009
Determine whether breakfast consumption is associated with adiposity in overweight Latino youth. Cross-sec
Berkey et al. 2003
Investigate whether breakfast skipping was associated with body fatness over 3 yr periods in the Growing Up Today Study
>14,000 boys and girls
Self reported
Chanyang et al. 2011
Assess the effects of skipping breakfast on diet quality in healthy
118 men and 297 women
Any food or beverage consumed in the morning
Results Days eating breakfast were predictive of lower BMI in models that adjusted for basic demographics. The independent effect of breakfast was no longer significant after parental education, energy intake, and physical activity were added to the model Breakfast omission was associated with IAAT independent of age, sex, tanner, total body fat, lean tissue, or energy intake
Notes Days eating breakfast were predictive of higher nutrient intake regardless of adjustment variables No association was found between breakfast and insulin secretion
The relationship between breakfast Overweight children who never and BMI is eat breakfast lost weight, but variable in normal weight children who children due to never eat breakfast gained weight growth. May not associate well with adult data Regular breakfast eaters Attribute benefit consumed more total calories of breakfast to than regular or rare breakfast improved nutrient
34
34
Table 1
Studies assessing the relationship between breakfast and body weight and/or total daily energy intake
Author
Elfhag et al. 2005
Keim et al. 1997
Appendix 1
Ma, Y et al. 2001
Research Design Korean adults Review of the literature on factors associated with weight loss maintenance (maintained for at least 6 months) and regain Determine whether large morning meals vs. large evening meals affects body weight or composition, RCT Evaluating eating patterns and obesity. Seasonal Variation of Blood Cholesterol Study
Analyze the differences between Ortega et al. the breakfast habits of 1998 obese, overweight, and normal weight schoolchildren
participants
Breakfast Definition
Results eater.
intake It is not clear if the factors for weight maintenance translate as helpful in weight loss Breakfast intake may influence weight loss distribution in fat and lean tissue
NA
Variable, self report
A regular meal rhythm that included breakfast was found to be a successful habit for weight maintenance
10 women
8-8:30 am controlled. 15% or 35% of total daily intake
Ingestion of larger AM meals resulted in slightly better weight loss but larger PM meals lead to better maintenance of fat-free mass
251 boys and 248 girls
118 boys and 82 girls
Notes
Self reported
skipping breakfast was associated with increased prevalence of obesity
Observed consumption during school breakfast
Obese children omitted breakfast more often. The energy supplied by breakfast, as a percentage of energy expenditure, was lower in obese children
Breakfast away from home and eating episodes was associated w/s risk of obesity. Obese children have less satisfactory breakfast habits and imbalanced energy profiles.
35
35
Table 1
Studies assessing the relationship between breakfast and body weight and/or total daily energy intake
Author
Research Design
Schlundt et al. 1992
Meals were provided as no breakfast, 2 meals/day, or 3 meals/day during weight loss
Szajewska et al. 2010
Review of the effects of breakfast on body weight in children and adolescents in Europe. All were cross sectional or cohort trials
Appendix 1
The assessment of Timlin et al. eating patterns and 2008 weight concerns among adolescents Van der Heijden et al. 2007 Wyatt, H. R. 2002
Breakfast consumption and long-term weight gain. Prospective Health Professionals Follow-up Study Examination of breakfast consumption in the
participants
52 women
≥ 59,000 children / adolescents in each trial
1007 boys 1215 girls
Breakfast Definition
Results
400 kcals or no breakfast but isocaloric daily intake
There was no main affect of breakfast and weight loss, but those who had to make the most substantial changes to their diet achieved better results.
variable
Thirteen studies showed that breakfast has a protective effect against becoming overweight or obese, and 4 studies showed an increase in BMI in breakfast skippers
Self reported
Frequency of breakfast was inversely associated with BMI in a dose-response manner
20,064 U.S. men
Self reported
607 men 2350 women
Self reported
Breakfast consumption was inversely associated with risk of 5kg weight gain after adjustment for age, this association was independent of lifestyle and BMI at baseline 2313 or 78%, reported regularly eating breakfast every day of the week. Only 114 subjects (4%)
Notes Eating breakfast was associated with decreased fat intake and compulsive snacking behavior All data was gathered from observational studies. Causality cannot be assumed Adjustment for weight-related factors partly explained the finding Fiber and nutrient intakes partially explained the association between breakfast and weight gain All participants maintained a weight loss of ≥
36
36
Table 1
Studies assessing the relationship between breakfast and body weight and/or total daily energy intake
Author
Research Design National Weight Control Registry
participants
Breakfast Definition
Results reported never eating breakfast
Notes 30 lbs for 1year.
Table 2 The effect of breakfast composition on subjective feelings of fullness, satiety-satiation, total daily calorie intake, and or weight-BMI
Appendix 1
Author
Research Design
Subjects
Barton et al. 2005
Changes in breakfast and cereal consumption and the association 2,379 girls of breakfast and cereal intake with body mass index
Bazzano, L. A. 2005
Assess the association between whole and refined grain breakfast cereal and risk of
17,881 males
Breakfast Definition
Results
Notes
Any eating between 5 AM and 10 AM on weekdays or 5 AM to 11 AM on weekends
Days eating cereal was predictive of lower BMI
Frequency of breakfast and cereal consumption decreased with age
Self reported
Men who consumed breakfast cereal, regardless of type, consistently weighed less than those who consumed breakfast
BMI and weight gain over 8 years were inversely associated with intake of breakfast cereals, independently of other risk factors. Physicians health
37
37
Table 2 The effect of breakfast composition on subjective feelings of fullness, satiety-satiation, total daily calorie intake, and or weight-BMI
Author
Research Design
Subjects
Breakfast Definition
Appendix 1
overweight and weight gain.
Results
Notes
cereals less often
Study
Self reported
Subjects who ate RTEC, cooked cereal, or quick breads for breakfast had significantly lower BMI compared to skippers and meat and egg eaters.
Breakfast skippers and fruit/vegetable eaters had the lowest daily energy intake. The meat and eggs eaters had the highest daily energy intake and one of the highest BMI’s. NHANES III
Cho, S. 2003
Investigate the relationship between breakfast type, energy intake and BMI
Clark,C.A. 2006
Evaluate a lowglycemic breakfast vs. a high-glycemic 75 males breakfast glucose, and 75 insulin, and free females fatty acid in response to a standard lunch
A high and low glycemic index breakfast. 30% of total energy needs
After the low Glycemic breakfast meal, post breakfast and post lunch AUC for plasma glucose and insulin were lower
A standard lunch which provided 30% of energy needs and was administered 4 hours after breakfast
Clegg, M. 2010
Examine how 9 Males macronutrient content at breakfast
Controlled breakfast provided: high-fat breakfast
Fullness increased and desire to eat decreased following the LFE
Both mass and energy content of food regulate subsequent appetite and feeding and
7687 males and 8765 females
38
38
Table 2 The effect of breakfast composition on subjective feelings of fullness, satiety-satiation, total daily calorie intake, and or weight-BMI
Author
Research Design
Subjects
effects gastric emptying and satiety RCT
Appendix 1
Assess different types of foods ingested at various de Castro, times of day with John M. 2009 total daily and macronutrient intakes. Crosssectional
DeshmukhTaskar, P. R. 2010
Examine the relationship between breakfast skipping and type consumed with nutrient intake, adequacy and adiposity status.
388 males, 621 females
9,659 males and females
Breakfast Definition (HF), LF breakfast isoenergetic to HF (LFE) and LF breakfast of equal mass to HF (LFM)
Results breakfast. Eating a HF breakfast increased the energy, fat and protein from the buffet.
Notes demonstrate the hyperphagic effect of a single HF meal.
Self reported
Eating low-density foods in High density foods were the morning and avoiding associated with greater total high-density foods at night daily intake. Coffee/tea had might aid in reducing overall a negative association with intake and may be useful in overall intake. dietary interventions for overweight and obesity.
Self reported
Prevalence of obesity (Body mass index ≥ 95th percentile) was higher in breakfast skippers than RTE cereal consumers and was higher in other breakfast consumers than RTE cereal consumers only
Children aged 9- 13 years (n= 4320) and adolescents aged 14- 18 years (n= 5339).
39
39
Table 2 The effect of breakfast composition on subjective feelings of fullness, satiety-satiation, total daily calorie intake, and or weight-BMI
Author
Appendix 1
Dubois et al. 2009
Research Design
Subjects
Breakfast Definition
Results
Notes
Cross-sectional
in adolescents.
Examine the association between skipping breakfast, daily energy, food intake, and BMI in pre-school children
Breakfast was not related to total daily energy intake, but breakfast skippers’ Breakfast may foster a more mean BMI increased as even distribution of energy energy intake, intake throughout the day carbohydrates increased, this was not true for breakfast eaters
775 boys 745 girls
Self report by parent
Compare the effects of a highinsoluble fiber cereal with low 16 males Hamedani, A. fiber cereal on food and 16 2009 intake, subjective females appetite, and plasma glucose in healthy individuals.
The HF cereal resulted in a Between 9-11am. higher subjective satiety 120 kcal for the HF per kcal, and lower cereal, 217 kcal for cumulative energy intake the LF cereal (from breakfast and lunch)
Holt, S.H
Four types realistic
Compare the
7 male, 7
Lunchtime food intake did not differ between cereals, but cumulative energy intake (cereal + lunch) was lower after the HF than after the LF cereal. A short-term benefit of the HF cereal, compared with LF cereal, was lower PG concentration before and immediately after lunch.
The high fiber carbohydrate The results confirm the
40
40
Table 2 The effect of breakfast composition on subjective feelings of fullness, satiety-satiation, total daily calorie intake, and or weight-BMI
Author
Appendix 1
1999
Research Design satiating property of foods. RCT
Leidy, H.J. 2010
Impact of normalprotein (PN) breakfast vs. protein-rich (PR) breakfast on appetite and food intake
Ortega, R.M. 1996
Gain knowledge and differences in breakfast habits were evaluated
Subjects female
7 males 6 females
65 males 57 females
Breakfast Definition isoenergetic breakfasts two fat rich and two carbohydrate rich
Results
Notes
rich breakfast was the most filling and was associated with less food intake during the morning and at lunch. Total daily calories were greater after the fat rich breakfast.
relatively weak satiating power of fat-rich meals. A high-fiber, carbohydrate-rich breakfast may assist weight control efforts by maintaining fullness. Average total energy intake was significantly greater after the fat-rich meal than after the high-fiber, carbohydrate-rich meal
Normal protein, protein rich, or breakfast skipping. 24% of estimated daily energy needs.
A breakfast rich in dietary Breakfast consumption lead protein provides additional to increased PYY and benefits through reductions in satiety regardless of protein appetite and energy intake. in composition. ‘breakfast-skipping’ adolescents.
Breakfast defined as all foods taken at first meal of the day, but always
Percentage of subjects whose breakfasts provided less than 20% of estimated energy expenditure was
In O subjects, breakfast provided lower percentage of recommended intake of fiber, vitamin E and iron. NW were
41
41
Table 2 The effect of breakfast composition on subjective feelings of fullness, satiety-satiation, total daily calorie intake, and or weight-BMI
Author
Research Design
Subjects
Appendix 1
between overweight (O) and normal weight (NW) elderly subjects.
Pereira, M.A. 2011
Examine effects of breakfast skipping and breakfast composition on blood glucose and appetite in children and adults (RCT).
Silberbauer, C. 1996
The effects of breakfasts with varying fiber and macronutrient content on satiety
9 males and females
18 males
Breakfast Definition before 11 a.m. foods consumed recorded as g per person per day.
Results
Notes
higher among O subjects, 62% compared to 45% in NW subjects.
more concerned with breakfast comp and their general state of health.
1 of four breakfast meals or water were provided: either high or low amounts of carbohydrates and high and low GI foods.
Glucose AUC was similar following the HCHG meal and skipping breakfast/water-only condition. GI did not effect glucose and insulin AUC when CHO was similar
Protein and energy were kept constant by modifying fat to achieve desired glycemic load. Participants were overweight, age 20-40
Standard isocaloric breakfast provided between 6:30am – 9:30am
Hunger, satiety, calories consumed at lunch, or time between meals was not affected by fiber or macronutrient content.
Results are consistent with the assumption that energy content of a meal is the major determinant of subsequent energy intake, fiber content and macronutrient composition have only a
42
42
Table 2 The effect of breakfast composition on subjective feelings of fullness, satiety-satiation, total daily calorie intake, and or weight-BMI
Author
Research Design
Subjects
Breakfast Definition
Results
Notes
Appendix 1
modulating effect.
Song, Won O. 2005
Test the hypothesis that breakfast consumption is associated with weight status (BMI) in US adults NHANES 19992000
Stubbs, R.J. 1996
To compare the effect of highprotein (HP), highfat (HF) or highcarbohydrate (HC) breakfasts on subjective hunger, fullness and appetite
4218 males and females
6 males
For women, the odds ratios Self reported for BMI >=25 were lower breakfast eaters: for breakfast consumers further classified as and RTEC breakfast RTEC or non consumers compared with RTEC breakfast breakfast non-consumers eaters and non-RTEC breakfast consumers.
Breakfasts provided at 8:30am and designed to match 75% of BMR
Subjective hunger was significantly greater during the hours between breakfast and lunch after the HF. The HP treatment suppressed hunger to a greater extent than the other two treatments.
For women, daily energy intake was higher among breakfast consumers than among breakfast non consumers
Large HP, HC or HF breakfasts led to detectable changes in hunger that were not of sufficient magnitude to influence lunch-time intake 5 h later, or EI for the rest of the day
43
43
Table 3 function
Breakfast consumption was not associated with one or all of the following: weight, food intake, and/or endocrine
Author/Year
Appendix 1
Abalkhail, B. 2002
Research Design Breakfast trends and the prevalence of anemia were investigated in schoolchildren and adolescents
Forslund, H. B. 2002
To characterize meal patterns in relation to obesity in Swedish women
Fujiwara, T. 2010
To examine the effect of skipping breakfast on reproductive function. In female college students aged from 18 to 20 years old
Participants
Breakfast Definition
2850 males and females
Not defined
177 females
A self reported meal between 6am– 10am excluding drink meals
975 females
Self reported food intake before 10am. Group I: breakfast every morning; II: one to six times a week; III, less than once a week
Results Skipping breakfast was reported by 14.9% of students and this habit did not differ by age, sex, body mass index or social class. No difference in breakfast consumption or frequency was found between obese and normal weight women
BMI was not different between breakfast consumption groups.
Notes Skipping breakfast was more marked among students with poor school performance as compared to those with very good or excellent results. A new simplified method assessing meal pattern revealed that the number of reported intake occasions across a usual day was higher in obese women compared with controls and the timing was shifted to later in the day. Despite no difference in body mass index, there was a significantly higher incidence of a selfperception of poor general health among the group that skipped breakfast
44
44
Table 3 function
Breakfast consumption was not associated with one or all of the following: weight, food intake, and/or endocrine
Author/Year Huang, Y.L. 1997
Morgan, K.J. 1986
Appendix 1
Ortega, R.M. 1996
Sampson, A.E. 1995
Research Design Breakfast consumption and daily fat and fiber intakes of young adults Examine the breakfast consumption patterns of the U.S. adult population through the USDA Nationwide consumption survey. longitudinal/cross sectional analysis To assess the relationships between concern over bodyweight, anthropometric parameters and energy balance To determine the contribution of breakfast-eating
Participants
Results No difference in age BMI, physical activity, and energy intake between breakfast eaters and skippers
Notes Breakfast is the meal lowest in fat and moderate in fiber content compared to other meals consumed by young adults
Any food or beverage between 5am and 10am
There was no difference in daily energy intake between breakfast eating groups, but adults who regularly eat RTEC consumed less fat and cholesterol
Results indicated that approximately one-quarter of the adult population skipped breakfast regularly. omission of breakfast had a significant negative impact, particularly among adult females, on diet quality
126 females
Self reported
Breakfast frequency was not different between obese and normal weight participants
30 day prospective analysis.
585 male and 566 female
Children’s self reported intake of food or beverage
Breakfast eating behavior was not associated with
Thirty-six percent of the children were obese, which did not vary with breakfast-
817 males, 1811females
15,959 males and females
Breakfast Definition Self reported, not defined
45
45
Table 3 function
Breakfast consumption was not associated with one or all of the following: weight, food intake, and/or endocrine
Appendix 1
Author/Year
Research Design behavior to dietary adequacy among low-income African-American children
Participants
Breakfast Definition Results before arriving to prevalence of school childhood obesity in this group of low income African American children.
Meal frequency and a First meal provided at period of fasting have 9am, but differed in no major impact on calorie level energy intake or expenditure
Taylor, M.A. 2001
The effect of a diet varying in energy, meal timing, or a morning fast
Williams, P. 2005
Describe nutrient intakes, and health of regular breakfast eaters and breakfast skippers.
10,851 males and females
Self reported
There was no difference between the fat intake or the body mass index of regular breakfast eaters compared with breakfast skippers
Williams, P. 2007
Describe nutrient intakes, and health
3,007 boys and girls
Self reported, 2-14 y of age by guardian
There was no difference between the
26 females
Notes eating behavior. Children who skipped breakfast compared to those who ate breakfast failed to achieve dietary adequacy for nearly every nutrient studied A morning fast resulted in a diet which tended to have a lower percentage of energy from carbohydrate than with no fast. Women had a BMI of greater than 25 kg/m2. Energy expenditure is delayed with a lower meal frequency compared with a higher meal frequency. Regular breakfast eaters were more likely to rate their health as excellent or good than those who skip breakfast. People who did not eat breakfast cereal were much more likely to have inadequate nutrient intakes The typical breakfast consumed was low in fat,
46
46
Table 3 function
Breakfast consumption was not associated with one or all of the following: weight, food intake, and/or endocrine
Appendix 1
Author/Year
Research Design of regular breakfast eaters and breakfast skippers
Participants
Breakfast Definition
Results fat intake and the body mass index of regular breakfast eaters compared with breakfast skippers
Notes high in carbohydrate and a good source of nutrients
47 Chapter 2
Habitual breakfast skipping is associated with fasting insulin resistance1, 2 Shavawn Forester3, Megan Witbracht4, Marinelle Nunez3, Peter Havel3, Kimber Stanhope3, James Graham3, William Horn4, Nancy Keim3, 4* 3
Department of Nutrition, 1 Shields Ave., University California, Davis, CA, USA 95616
4
U.S. Department of Agriculture, Agricultural Research Service, Western Human Nutrition
Research Center, Obesity and Metabolism Research Unit, Davis, CA, USA 95616
1
This project has been funded by Denka Seiken Co.& Otsuka Pharmaceutical Co., Ltd. Tokyo,
Japan and USDA-CRIS 5306 51530 019 2
Author disclosures: S. M. Forester has no conflicts of interest to report
48 Abstract Health professionals recommend breakfast as an important part of healthy eating, but current research has not clearly identified the metabolic advantages associated with breakfast eating. Three intervention trials have reported that forced breakfast skipping led to a blunted postprandial insulin response. Our aim was to examine, in a cross sectional design, if selfreported habitual breakfast skipping was related to fasting insulin resistance (Homeostatic Model Assessment HOMA2-IR) in a sample of 321 adults, aged 21-75 y, BMI 18.06-29.86 kg/m2. Subjects responded to a questionnaire that focused on eating occurrences through the day and were classified by how frequently they ate breakfast: 81% were regular breakfast eaters (Br-E) 7 days/week, 12% ate intermittently (Br-I) 3-6 days/week, and 7% skipped breakfast (Br-S) 1 day/week or less. Initial analysis of variance revealed that breakfast eating was related to fasting insulin (p