Endogenous circadian system and circadian misalignment impact glucose tolerance via separate mechanisms in humans

Apr 15, 2015Proceedings of the National Academy of Sciences of the United States of America

Internal body clock and its mismatch affect blood sugar control in different ways in people

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Abstract

Postprandial glucose was 17% higher in the biological evening compared to the morning.

Glucose tolerance is lower in the evening and at night than in the morning.
The circadian system and circadian misalignment have distinct impacts on glucose tolerance, independent of the behavioral cycle.
Circadian misalignment (12-h behavioral cycle inversion) led to a 6% increase in postprandial glucose.
Decreased pancreatic β-cell function accounted for reduced insulin response during the biological evening.
Circadian misalignment was associated with decreased insulin sensitivity, evidenced by elevated postprandial glucose levels despite higher late-phase insulin.

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Glucose tolerance is lower in the evening and at night than in the morning. However, the relative contribution of the circadian system vs. the behavioral cycle (including the sleep/wake and fasting/feeding cycles) is unclear. Furthermore, although shift work is a diabetes risk factor, the separate impact on glucose tolerance of the behavioral cycle, circadian phase, and circadian disruption (i.e., misalignment between the central circadian pacemaker and the behavioral cycle) has not been systematically studied. Here we show--by using two 8-d laboratory protocols--in healthy adults that the circadian system and circadian misalignment have distinct influences on glucose tolerance, both separate from the behavioral cycle. First, postprandial glucose was 17% higher (i.e., lower glucose tolerance) in the biological evening (8:00 PM) than morning (8:00 AM; i.e., a circadian phase effect), independent of the behavioral cycle effect. Second, circadian misalignment itself (12-h behavioral cycle inversion) increased postprandial glucose by 6%. Third, these variations in glucose tolerance appeared to be explained, at least in part, by different mechanisms: during the biological evening by decreased pancreatic β-cell function (27% lower early-phase insulin) and during circadian misalignment presumably by decreased insulin sensitivity (elevated postprandial glucose despite 14% higher late-phase insulin) without change in early-phase insulin. We explored possible contributing factors, including changes in polysomnographic sleep and 24-h hormonal profiles. We demonstrate that the circadian system importantly contributes to the reduced glucose tolerance observed in the evening compared with the morning. Separately, circadian misalignment reduces glucose tolerance, providing a mechanism to help explain the increased diabetes risk in shift workers.

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Endogenous circadian system and circadian misalignment impact glucose tolerance via separate mechanisms in humans

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