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Time-of-day-dependent dietary fat consumption influences multiple cardiometabolic syndrome parameters in mice.

Bray MS, Tsai JY, Villegas-Montoya C, Boland BB, Blasier Z, Egbejimi O, Kueht M, Young ME - Int J Obes (Lond) (2010)

Bottom Line: Despite growing acceptance that biological rhythms profoundly influence energy homeostasis, little is known regarding how the timing of nutrient ingestion influences development of common metabolic diseases.To test the hypothesis that the time of day at which dietary fat is consumed significantly influences multiple cardiometabolic syndrome parameters.The time of day at which carbohydrate versus fat is consumed markedly influences multiple cardiometabolic syndrome parameters.

View Article: PubMed Central - PubMed

Affiliation: Department of Epidemiology, University of Alabama at Birmingham, Birmingham, AL, USA.

ABSTRACT

Background: Excess caloric intake is strongly associated with the development of increased adiposity, glucose intolerance, insulin resistance, dyslipidemia, and hyperleptinemia (that is the cardiometabolic syndrome). Research efforts have focused attention primarily on the quality (that is nutritional content) and/or quantity of ingested calories as potential causes for diet-induced pathology. Despite growing acceptance that biological rhythms profoundly influence energy homeostasis, little is known regarding how the timing of nutrient ingestion influences development of common metabolic diseases.

Objective: To test the hypothesis that the time of day at which dietary fat is consumed significantly influences multiple cardiometabolic syndrome parameters.

Results: We report that mice fed either low- or high-fat diets in a contiguous manner during the 12  h awake/active period adjust both food intake and energy expenditure appropriately, such that metabolic parameters are maintained within a normal physiologic range. In contrast, fluctuation in dietary composition during the active period (as occurs in human beings) markedly influences whole body metabolic homeostasis. Mice fed a high-fat meal at the beginning of the active period retain metabolic flexibility in response to dietary challenges later in the active period (as revealed by indirect calorimetry). Conversely, consumption of high-fat meal at the end of the active phase leads to increased weight gain, adiposity, glucose intolerance, hyperinsulinemia, hypertriglyceridemia, and hyperleptinemia (that is cardiometabolic syndrome) in mice. The latter perturbations in energy/metabolic homeostasis are independent of daily total or fat-derived calories.

Conclusions: The time of day at which carbohydrate versus fat is consumed markedly influences multiple cardiometabolic syndrome parameters.

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Related in: MedlinePlus

Mice were divided into two distinct feeding groups, as depicted in Figure 1A. The effects of these feeding regimes on caloric intake (A), body weight (B), percent body fat (C), glucose tolerance (D), as well as energy expenditure, respiratory quotient, and physical activity (E) were determined. Data are shown as mean +/- SEM for 5-8 independent observations. * denotes p<0.05 main diet effect and $ denotes p<0.05 diet effect at a specific ZT.
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Figure 2: Mice were divided into two distinct feeding groups, as depicted in Figure 1A. The effects of these feeding regimes on caloric intake (A), body weight (B), percent body fat (C), glucose tolerance (D), as well as energy expenditure, respiratory quotient, and physical activity (E) were determined. Data are shown as mean +/- SEM for 5-8 independent observations. * denotes p<0.05 main diet effect and $ denotes p<0.05 diet effect at a specific ZT.

Mentions: We and others have demonstrated that ad libitum high fat feeding (i.e., 45% calories from fat) for 12 weeks results in significantly increased body weight gain and adiposity in wild-type FVB/N mice, along with predicted alterations in whole body energy expenditure and metabolism, as well as decreased glucose tolerance (Supplementary Figures 1 and 2) (8-10). We subsequently investigated whether consumption of the high fat diet during the light versus the dark phase would influence these parameters, while taking care not to overtly disrupt circadian behavior. Mice were randomly assigned to one of two groups, as illustrated in Figure 1A. Mice in the light phase high fat (LPHF) group were provided the high fat diet during the light phase, followed by the control diet during the dark phase. Mice in the dark phase high fat (DPHF) group were provided the control diet during the light phase, followed by the high fat diet during the dark phase. Food was available ad libitum during both phases. Although daily total caloric intake did not differ between the two groups, DPHF mice consumed more fat-derived calories compared to LPHF mice (Figure 2A). A large proportion of the dietary fat consumed occurred at the initiation of dark phase and light phase for DPHF and LPHF mice respectively (Figure 2A and Supplementary Figure 3). No significant differences were observed for body weight or body composition between LPHF and DPHF mice after 12 weeks of the feeding regime (Figures 2B and 2C). In addition, no significant differences were observed for glucose tolerance between mice in these two feeding groups (Figure 2D). Indirect calorimetry exposed higher oxygen consumption and energy expenditure in DPHF mice, compared to LPHF mice (Figure 2E and Supplementary Figure 3). This did not appear to be due to differences in physical activity (Figure 2E and Supplementary Figure 3). These data suggest that, during extended periods of a contiguous diet, animals are able to adequately adjust whole body homeostasis, allowing for excess dietary lipid ingestion.


Time-of-day-dependent dietary fat consumption influences multiple cardiometabolic syndrome parameters in mice.

Bray MS, Tsai JY, Villegas-Montoya C, Boland BB, Blasier Z, Egbejimi O, Kueht M, Young ME - Int J Obes (Lond) (2010)

Mice were divided into two distinct feeding groups, as depicted in Figure 1A. The effects of these feeding regimes on caloric intake (A), body weight (B), percent body fat (C), glucose tolerance (D), as well as energy expenditure, respiratory quotient, and physical activity (E) were determined. Data are shown as mean +/- SEM for 5-8 independent observations. * denotes p<0.05 main diet effect and $ denotes p<0.05 diet effect at a specific ZT.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3021134&req=5

Figure 2: Mice were divided into two distinct feeding groups, as depicted in Figure 1A. The effects of these feeding regimes on caloric intake (A), body weight (B), percent body fat (C), glucose tolerance (D), as well as energy expenditure, respiratory quotient, and physical activity (E) were determined. Data are shown as mean +/- SEM for 5-8 independent observations. * denotes p<0.05 main diet effect and $ denotes p<0.05 diet effect at a specific ZT.
Mentions: We and others have demonstrated that ad libitum high fat feeding (i.e., 45% calories from fat) for 12 weeks results in significantly increased body weight gain and adiposity in wild-type FVB/N mice, along with predicted alterations in whole body energy expenditure and metabolism, as well as decreased glucose tolerance (Supplementary Figures 1 and 2) (8-10). We subsequently investigated whether consumption of the high fat diet during the light versus the dark phase would influence these parameters, while taking care not to overtly disrupt circadian behavior. Mice were randomly assigned to one of two groups, as illustrated in Figure 1A. Mice in the light phase high fat (LPHF) group were provided the high fat diet during the light phase, followed by the control diet during the dark phase. Mice in the dark phase high fat (DPHF) group were provided the control diet during the light phase, followed by the high fat diet during the dark phase. Food was available ad libitum during both phases. Although daily total caloric intake did not differ between the two groups, DPHF mice consumed more fat-derived calories compared to LPHF mice (Figure 2A). A large proportion of the dietary fat consumed occurred at the initiation of dark phase and light phase for DPHF and LPHF mice respectively (Figure 2A and Supplementary Figure 3). No significant differences were observed for body weight or body composition between LPHF and DPHF mice after 12 weeks of the feeding regime (Figures 2B and 2C). In addition, no significant differences were observed for glucose tolerance between mice in these two feeding groups (Figure 2D). Indirect calorimetry exposed higher oxygen consumption and energy expenditure in DPHF mice, compared to LPHF mice (Figure 2E and Supplementary Figure 3). This did not appear to be due to differences in physical activity (Figure 2E and Supplementary Figure 3). These data suggest that, during extended periods of a contiguous diet, animals are able to adequately adjust whole body homeostasis, allowing for excess dietary lipid ingestion.

Bottom Line: Despite growing acceptance that biological rhythms profoundly influence energy homeostasis, little is known regarding how the timing of nutrient ingestion influences development of common metabolic diseases.To test the hypothesis that the time of day at which dietary fat is consumed significantly influences multiple cardiometabolic syndrome parameters.The time of day at which carbohydrate versus fat is consumed markedly influences multiple cardiometabolic syndrome parameters.

View Article: PubMed Central - PubMed

Affiliation: Department of Epidemiology, University of Alabama at Birmingham, Birmingham, AL, USA.

ABSTRACT

Background: Excess caloric intake is strongly associated with the development of increased adiposity, glucose intolerance, insulin resistance, dyslipidemia, and hyperleptinemia (that is the cardiometabolic syndrome). Research efforts have focused attention primarily on the quality (that is nutritional content) and/or quantity of ingested calories as potential causes for diet-induced pathology. Despite growing acceptance that biological rhythms profoundly influence energy homeostasis, little is known regarding how the timing of nutrient ingestion influences development of common metabolic diseases.

Objective: To test the hypothesis that the time of day at which dietary fat is consumed significantly influences multiple cardiometabolic syndrome parameters.

Results: We report that mice fed either low- or high-fat diets in a contiguous manner during the 12  h awake/active period adjust both food intake and energy expenditure appropriately, such that metabolic parameters are maintained within a normal physiologic range. In contrast, fluctuation in dietary composition during the active period (as occurs in human beings) markedly influences whole body metabolic homeostasis. Mice fed a high-fat meal at the beginning of the active period retain metabolic flexibility in response to dietary challenges later in the active period (as revealed by indirect calorimetry). Conversely, consumption of high-fat meal at the end of the active phase leads to increased weight gain, adiposity, glucose intolerance, hyperinsulinemia, hypertriglyceridemia, and hyperleptinemia (that is cardiometabolic syndrome) in mice. The latter perturbations in energy/metabolic homeostasis are independent of daily total or fat-derived calories.

Conclusions: The time of day at which carbohydrate versus fat is consumed markedly influences multiple cardiometabolic syndrome parameters.

Show MeSH
Related in: MedlinePlus