The Human Circadian System Has a Dominating Role in Causing the Morning/Evening Difference in Diet-Induced Thermogenesis

Abstract

Objective: Diet-induced thermogenesis (DIT) is lower in the evening and at night than in the morning. This may help explain why meal timing affects body weight regulation and why shift work is a risk factor for obesity. The separate effects of the endogenous circadian system--independent of behavioral cycles--and of circadian misalignment on DIT are unknown.

Methods: Thirteen healthy adults undertook a randomized crossover study with two 8-day laboratory visits: three baseline days followed either by repeated simulated night shifts including 12-h inverted behavioral cycles (circadian misalignment) or by recurring simulated day shifts (circadian alignment). DIT was determined for up to 114 min (hereafter referred to as "early DIT") following identical meals given at 8AM and 8PM in both protocols.

Results: During baseline days, early DIT was 44% lower in the evening than morning. This was primarily explained by a circadian influence rather than any behavioral cycle effect; early DIT was 50% lower in the biological evening than biological morning, independent of behavioral cycle influences. Circadian misalignment had no overall effect on early DIT.

Conclusions: The circadian system plays a dominating role in the morning/evening difference in early DIT and may contribute to the effects of meal timing on body weight regulation.

© 2015 The Obesity Society.

Figures

Fig. 1. Circadian alignment protocol (top panel) and circadian misalignment protocol (bottom panel)

On day 1 in both protocols, participants received an ad libitum lunch at approximately 12PM. Caloric intake was prorated for the 12-h behavioral cycle on day 4 of the circadian misalignment protocol (i.e., they received 50% of the caloric content as compared to the other 24-h days). Light levels indicated are in the horizontal angle of gaze: ~90 lux, to simulate typical room light intensity, ~450 lux during the first three baseline wake episodes to enhance circadian entrainment, 30-min periods of ~450 lux to simulate the morning commute both preceding the day work shift (circadian alignment protocol) and following the night work shift (circadian misalignment protocol)—this was expected to oppose the central circadian pacemaker from delaying its phase during the circadian misalignment protocol (31), ~4 lux to permit assessment of the dim-light melatonin onset; 0 lux during scheduled sleep episodes. Light levels during test meal assessments were 450 lux on baseline days and 90 lux on experimental days. Light blue bars represent meals and snacks (narrow bar). Green bars represent test meal assessments, with the test meals consumed within the first 20 min. The letters B and D indicate breakfast and dinner, respectively. Numbers following B or D indicate test days (first or third) and letters following these numbers indicate whether the test meals were consumed during circadian alignment (A) or circadian misalignment (M). To graphically represent the independent effects of the behavioral cycle, circadian phase and circadian misalignment in subsequent figures, we (1) averaged breakfast time (BA and BM) and dinner time (DA and DM) test meal values separately across both protocols for each test day (behavioral cycle effect); (2) averaged 8AM (BA and DM) and 8PM (DA and BM) test meal values separately across both protocols for each test day (circadian phase effect); and (3) averaged alignment (BA and DA) and misalignment (BM and DM) test meal values within each protocol for each test day (circadian misalignment effect).

Fig. 2. Baseline days (n=13); Early diet-induced thermogenesis (DIT, top panel), absolute early postprandial energy expenditure (postprandial EE, middle panel) and resting energy expenditure (REE, bottom panel) during the morning and evening test sessions during a normal sleep/wake cycle

Data are represented as mean±SEM.

Fig. 3. Experimental days (n=11); Effects of the behavioral cycle (left panel), circadian phase (middle panel) and circadian misalignment (right panel) on early diet-induced thermogenesis (DIT)

Data are derived as described in the legend of Fig. 1. Data are represented as mean±SEM.

Fig. 4. Experimental days (n=11); Effects of the behavioral cycle (left panel), circadian phase (middle panel) and circadian misalignment (right panel) on absolute early postprandial energy expenditure (postprandial EE)

Data are derived as described in the legend of Fig. 1. Data are represented as mean±SEM.

Fig. 5. Experimental days (n=11); Effects of the behavioral cycle (left panel), circadian phase (middle panel) and circadian misalignment (right panel) on resting energy expenditure (REE)

Data are derived as described in the legend of Fig. 1. Data are represented as mean±SEM.