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ScienceDirect Circadian rhythms and meal timing: impact on energy balance and body weight Hedda L Boege1, Mehreen Z Bhatti1 and Marie-Pierre St-Onge1,2 Energy metabolism and appetite regulating hormones follow circadian rhythms which, when disrupted, could lead to adverse metabolic consequences. Such circadian misalignment, a mismatch between endogenous circadian rhythms and behavior, is most severely experienced by shift workers, due to nighttime wake, daytime sleep, and eating at night. However, circadian misalignment is not restricted to shift workers; milder shifts in sleep and mealtimes, termed social and eating jetlag, are highly prevalent in the general population. Social and eating jetlag result in later mealtimes, which may promote positive energy balance and weight gain. Earlier meal timing, specific to individual endogenous circadian patterns, could serve to reduce cardiometabolic disease burden and aid in weight loss and interventions should be done to test this. Addresses 1 Sleep Center of Excellence and Division of General Medicine, Department of Medicine, Columbia University Irving Medical Center, New York, NY, USA 2
Institute of Human Nutrition, Columbia University Irving Medical Center, New York, NY, USA
Corresponding author: St-Onge, Marie-Pierre ([email protected]
Current Opinion in Biotechnology 2021, 70:xx–yy This review comes from a themed issue on Food biotechnology Edited by Anna E Thalacker-Mercer and Martha Field
https://doi.org/10.1016/j.copbio.2020.08.009 0958-1669/ã 2020 Elsevier Ltd. All rights reserved.
Introduction Circadian rhythms are cyclic endogenous biological patterns following an 24-hour cycle that regulate the timing of physiology, metabolism, and behavior. They initiate wake and sleep episodes at the appropriate biological time as well as signal feeding and fasting. When behaviors such as eating and sleeping fail to align with circadian cues, misalignment can occur, compromising the integrity of robust endogenous circadian rhythms . Repeated disruption through mismatched timing of eating and sleeping has been shown to increase the risk of obesity, type 2 diabetes and cardiovascular disease [1,2]. Correspondingly, shift workers, who experience chronic www.sciencedirect.com
circadian misalignment due to complete reversal of feeding-fasting and wake-sleep behavioral cycles, provide the strongest evidence for these effects . Milder desynchronizing behavioral patterns, such as variability in sleep and meal times throughout the week, are highly prevalent in modern society and have been coined social  and eating  jetlag (differences in the midpoint of the sleep or feeding episode on free days versus work days) (Figure 1). The timing of food intake, particularly, has come to the forefront of research efforts with studies showing that consumption of food later in the day and closer to bedtime is associated with higher weight status [6,7]. While still in early stages, findings from this field of study have broad applicability. The demands of modern life result in many non-shift workers delaying morning meals, adopting irregular eating patterns and extending eating into the night [8–10]. Adjustment of meal timing in accordance with individual endogenous circadian rhythms could serve to reduce cardiometabolic disease burden. Here we present evidence on the effect of meal timing, as a disruptor of circadian rhythms, on energy balance (energy intake and energy expenditure) and body weight. Research to date has focused on leptin and ghrelin as regulators of food intake, and resting energy expenditure, all of which are known to exhibit circadian rhythmicity [11–13].
Entrainment of circadian clocks and circadian alignment The endogenous circadian system is primarily controlled by an autonomous master clock in the suprachiasmatic nucleus (SCN) of the hypothalamus, which is synchronized by ambient light and entrains secondary clocks in the brain and most peripheral tissues of the body . Importantly, secondary clocks are also entrained by environmental cues and behaviors, termed ‘zeitgebers,’ such as eating and sleeping [1,2]. When environmental and behavioral factors are repeatedly misaligned from the SCN-driven endogenous circadian cycle, such as when food intake occurs during the night, integration of mistimed signals can disrupt the tightly controlled peripheral system, resulting in a loss of homeostasis (circadian misalignment) . Meanwhile, in conditions of circadian alignment, behavioral cues feed into peripheral circadian systems at the appropriate phase, facilitating the smooth cycling of physiological processes (Figure 1). The circadian rhythms of appetite regulating hormones, energy expenditure and substrate utilization prepare the body for Current Opinion in Biotechnology 2021, 70:1–6
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An overview of how mistimed sleeping and eating result in circadian misalignment and the metabolic consequences. (a) The circadian system promotes wakefulness/feeding during the biological day and sleep/fasting during the biological night. (b) Several behavioral patterns do not fit these endogenous preferences. Shift work: Awake/feeding at night and sleeping/fasting during the day, causing severe circadian misalignment. Social Jetlag: A shift in the midpoint of sleep on workdays versus free days, causing mild circadian misalignment. Eating jetlag: A shift in the midpoint of the feeding episode on workdays versus free days, causing mild circadian misalignment. These behavioral patterns result in a mismatch between the timing of eating/sleeping and the endogenous circadian system (indicated in magenta). Circadian misalignment is thought to disrupt energy balance, resulting in increased body weight and cardiometabolic risk.
specific biological responses at different times of day to maintain energy balance. For example, ghrelin levels are higher in the biological evening than the morning , promoting greater evening hunger. In contrast, diet induced thermogenesis (DIT), the rise in energy expenditure after a meal, is higher after a morning meal than after an isocaloric evening meal [14,15], indicating more calories burned after a morning meal. Respiratory quotient (RQ), an index of macronutrient utilization, is highest in the biological morning, indicative of greater carbohydrate oxidation, and lowest during the biological evening, indicating greater lipid oxidation [11,16]. These rhythms have implications for health and mismatched behaviors in relation to these endogenous processes can result in adverse health effects.
Severe circadian desynchronization Studies in mice have shown that food intake during the biological night, akin to night shift work in humans, causes a 12-hour shift in peripheral clock, but not central clock, activity . Such mistimed feeding results in higher body weight  and increased risk of metabolic Current Opinion in Biotechnology 2021, 70:1–6
syndrome and diabetes  relative to control mice fed during the biological day. Studies in humans have similarly shown phase shifts in peripheral clock activity in response to inappropriate timing of sleep and food intake, while the phase of the SCN master clock remains unaffected [3,19]. Chronic shift work has been associated with metabolic disruption and positive energy balance, resulting in increased risk of obesity, type 2 diabetes, heart disease and metabolic syndrome . The largest body of evidence for the impact of circadian misalignment on human health stems from clinical interventions approximating the conditions of shift work in healthy, non-shift working volunteers. Acute circadian misalignment is induced via simulated night shift or forced desynchrony protocols, in which either active and rest phases are reversed, or the day is artificially shortened/extended. This effectively shifts the behavioral patterns of sleep and eating out of phase with the endogenous rhythm of the SCN master clock, substantially altering the input received by peripheral clocks that regulate metabolism . www.sciencedirect.com
Circadian rhythms, meal timing, and body weight
One proposed contributor to the increased risk of obesity observed in shift workers is higher energy intake due to altered levels of hunger and satiety hormones ghrelin and leptin in response to circadian misalignment. Multiple simulated shiftwork studies observed decreased leptin levels [21–24,25] and increased ghrelin levels [12,21,25,26] in circadian misalignment relative to circadian alignment conditions. According to a recent study , these effects may be sex-dependent. Indeed, night shift work (circadian misalignment) induced a 7% decrease in 24-hour leptin levels and an 8% increase in wake period ghrelin levels in females whereas in males, leptin levels were increased by 11% and ghrelin levels were unchanged compared to the daytime work (circadian aligned) condition . Increased hunger and decreased satiety in response to circadian misalignment and depending on time of eating could contribute to weight gain in shift workers  and late eaters . Meanwhile, despite higher risk of obesity and chronic disorders, studies have not reported significant differences in energy intake between shift and non-shift workers by objective measure  or self-report [29,30,31]. However, this could reflect inherent biases in food intake measures . Whereas the influence of circadian misalignment on food intake regulation is more conclusive, evidence related to energy expenditure is more equivocal. A simulated night shift intervention showed a small but significant reduction in 24-hour resting energy expenditure (REE) after circadian misalignment compared to alignment , while similar protocols produced an increase  or no effect [11,23]. The discordance in results could be explained by the finding that REE differs greatly between individuals but is very stable within a person . These inter-individual differences may be in part driven by sex: Qian et al.  observed distinct sexspecific differences, with REE increasing by 4.5% in females after circadian misalignment, while there was no change in males. Circadian misalignment may also affect substrate utilization. Compared to circadian alignment, misalignment results in reduced RQ [11,16,25], with concomitant lower carbohydrate oxidation [16,24] and higher lipid oxidation [16,24]. There is some evidence that this effect may also be sex-specific, with reduced RQ being observed in females but not in males . In general, the circadian system favors carbohydrate utilization in the biological morning and lipid utilization in the biological evening [11,16]. Circadian misalignment may cause a potentially unfavorable shift in these patterns when considered in conjunction with other circadian-controlled metabolic processes, such as glucose regulation. Indeed, multiple clinical interventions have demonstrated disrupted glucose-insulin metabolism in response to acute circadian misalignment. Postprandial glucose levels are raised in response to misaligned mealtimes and insulin www.sciencedirect.com
sensitivity is reduced [16,22,23], which may increase risk of type 2 diabetes.
Milder circadian desynchronization Epidemiological studies show that individuals with greater social jetlag (difference in midpoint of the sleep period between work and free days) have higher BMI, adiposity and odds of obesity, metabolic syndrome and type 2 diabetes [34,35]. In a study population with obesity-related chronic diseases, greater social jetlag was associated with consumption of more calories, saturated fat and cholesterol at dinner, of more protein, total fat, saturated fat and cholesterol at lunch, as well as more total fat and saturated fat consumed at morning snack . Because of later waking times, social jetlag was also associated with later mealtimes for breakfast, early afternoon snack and dinner . These later consumption patterns, at odds with endogenous preference, could contribute to the observed risk of obesity in those with greater social jetlag. Few clinical intervention studies have explored the metabolic effects of mild circadian misalignment. One observational study showed that those with later midpoint of sleep, but not necessarily social jetlag, had higher energy intakes at dinner and after 8 PM, behaviors that were associated with higher BMI, as well as higher intakes of fast food, sugar-sweetened beverages, and lower fruits and vegetables . However, this study was confounded by differences in sleep duration, whereby those with later sleep times also had shorter sleep duration than those with earlier sleep times. We and others have shown that short sleep duration increases food intake [37,38]. Another study showed that sleep restriction for two nights followed by two nights of sleep recovery and another two nights of sleep restriction, effectively shifting midpoint of sleep by 2.5 hours between sleep restriction and sleep recovery, increases food intake relative to baseline, prestudy sleep . Both periods of sleep restriction increased energy intakes by 1000 kcal whereas recovery sleep increased intakes by 500 kcal relative to baseline. Sex differences were observed whereby intakes were increased similarly in the two sleep restriction periods in both men and women, but intakes during recovery sleep returned to baseline levels in women only. However, this study too, was confounded by differences in sleep duration throughout the sleep conditions . Our lab attempted to address this research gap via a 4phase randomized crossover pilot study with constant sleep duration . Six men and women underwent four inpatient phases in which the timing, but not duration, of sleep and meals was manipulated: Normal sleep/normal meals, normal sleep/late meals, late sleep/normal meals and late sleep/late meals. Sleep and mealtimes were delayed by 3.5 hours in the late conditions relative to those with normal times. Glucagon-like peptide Current Opinion in Biotechnology 2021, 70:1–6
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1 concentrations in response to a meal were higher with early sleep and mealtimes, suggesting improved satiety compared with the late meal condition . In contrast, earlier sleep and mealtimes were associated with higher ghrelin concentrations and did not influence leptin concentrations. The combination of normal sleep and mealtimes had a reducing effect on food intakes . Although limited, these studies suggest a potential influence of small shifts in sleep and meal timing on regulation of energy balance. We are not aware of any study that has assessed the influence of social jetlag on REE.
Meal timing and weight status Outside of the laboratory, several recent epidemiological studies have examined the association between timing of eating and obesity risk. Eating jetlag, the difference in midpoint of the eating period between work and free days, has been associated with higher BMI . In this epidemiological sample, eating jetlag was driven primarily by a delay in breakfast time on weekends relative to weekdays. Later meal timing in general has been associated with higher daily caloric intakes  and higher BMI, independent of sleep timing and duration . Xiao et al.  associated a higher percentage of dietary intake in the morning with 50% lower odds of overweight or obesity, while a higher percentage of dietary intake in the evening was associated with 80% higher odds of overweight or obesity. A study by Bandı´n et al.  in which mealtimes were delayed by 3.5 hours while sleep was kept constant, showed decreased pre-meal REE, decreased fasting RQ and decreased carbohydrate oxidation compared to the control condition. Other studies have shown that dietinduced thermogenesis (DIT), the rise in energy expenditure in response to food intake, is consistently lower in response to an evening meal compared with a morning meal [14,15,24]. In fact, one study reported 44% lower DIT following an evening meal compared to a morning meal . These findings suggest that energy homeostasis is favored when greater caloric intakes occur in the morning/early afternoon versus the evening/night due to higher energy costs of processing foods consumed at an earlier time. Importantly, meal timing patterns may not follow a ‘onesize-fits-all’ approach. Recent findings suggest that timing of meals relative to individual circadian clock timing, marked by evening melatonin onset, is a better predictor of body composition and weight status than clock time [42,43]. Indeed, individuals consuming a greater proportion of their daily energy intakes closer to melatonin onset (circadian clock) had higher BMI and percentage body fat than those who consumed food earlier in their biological day . The same study showed that individuals with higher percentage body fat ate 8% more of their total daily calories in the biological evening, and 13% Current Opinion in Biotechnology 2021, 70:1–6
more carbohydrates in the biological afternoon, irrespective of clock hour, than individuals with lower percentage body fat . Given the circadian rhythmicity of DIT and substrate oxidation highlighted above, food consumption later in the day could result in fewer calories burned and greater carbohydrates remaining in circulation, increasing the risk of weight gain and type 2 diabetes in susceptible individuals.
Meal timing and weight loss Given the associations between timing of food intake and circadian alignment, it is plausible that shifting mealtimes could influence weight management. Indeed, behavioral weight loss programs have shown that greater weight loss occurs in those who consume their main daily meal earlier in the day compared to those who consume that meal later in the day  and in those who consume the greatest percentage of daily calories during a morning meal [45– 48]. A six-year follow-up study of bariatric surgery similarly associated earlier consumption of the main meal with greater weight loss success compared to a later main meal, an observation that could not be explained by differences in energy intake, diet composition or sleep duration . These results indicate that the timing of meals and distribution of caloric intake throughout the day may be important considerations for weight management, along with traditional dietary characteristics such as energy intake and diet composition.
Conclusion Circadian misalignment is increasingly recognized as a risk factor for obesity and cardiometabolic disease. While shift workers are most affected, there is a growing understanding that milder shifts in eating and sleeping patterns, such as social jetlag and eating jetlag, can also have adverse health consequences. Both social and eating jetlags result in later meal consumption patterns, which may result in eating at biologically unfavorable times for energy and macronutrient metabolism. Clinical intervention studies assessing the effects of these subtle shifts in sleep and meal timing are needed to uncover the mechanism by which mild forms of circadian misalignment lead to higher body weight and cardiometabolic risk. Finally, due to inter-individual differences in circadian timing, it may be important to personalize meal timing recommendations. Meal timing in relation to chronotype, a measure of innate individual preference for morning or evening shown to modulate the risk associated with late eating , could be considered to alleviate burden in those at high risk. An understanding of circadian rhythms and differential metabolic responses to food intake at different circadian phases can inform recommendations for temporally healthier eating patterns and should be the subject of clinical investigations.
Conflict of interest statement Nothing declared. www.sciencedirect.com
Circadian rhythms, meal timing, and body weight
Acknowledgements This was funded in part by the National Institutes of Health [grant numbers R01 HL142648, R01 HL128226] and the American Heart Association [grant number 16SFRN27950012] (St-Onge).
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