The Implications of Eating or Skipping Breakfast: Physiology, Behavior, and the Satiety Hormone Response

The Implications of Eating or Skipping Breakfast: Physiology, Behavior, and the Satiety Hormone Response SHAVAWN MARIE FORESTER B.S. (University of C...
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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

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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

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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

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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!

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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

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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.

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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.

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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

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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.

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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.

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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:

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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

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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).

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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

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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

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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

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