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Diurnal variation in glucose tolerance. Cyclic suppression of insulin action and insulin secretion in normal-weight, but not obese, subjects
Abstract
The relative roles of insulin sensitivity, insulin secretion, and glucose effectiveness to the diurnal rhythm of glucose tolerance were examined in normal-weight (n = 12) and obese (n = 11) subjects. Two frequently sampled intravenous glucose tolerance tests were performed in each subject at 0800 on one occasion and 1800 on a separate day. Tests were preceded by identical fasts of 10–12 h. In nonobese subjects, glucose tolerance, expressed as the 10- to 16-min KG value (KGS), was much reduced in the evening (AM 2.98 ± 0.45, PM 1.86 ± 0.33 min−1 P < 0.002). In the obese subjects, tolerance was lower in the morning than normal-weight subjects (2.19 ± 0.31 min−1), but unlike in nonobese subjects, tolerance was not significantly reduced during the day (1.90 ± 0.18 min−1 P > 0.40). The reduction in glucose tolerance in the normal-weight subjects was caused by diminished insulin sensitivity (parameter S1, AM 15.4 ± 2.9, PM 10.2 ± 1.9 × 10−5 min−1/pM, P < 0.01) and reduced β-cell responsivity to glucose. The evening decrease in the latter was reflected both in first-phase plasma insulin (AM 2466 ± 441, PM 1825 ± 381 pM/10 min, P < 0.05) and the potentiation slope (AM 462 ± 68, PM 267 ± 35 pM/mM, P < 0.01). In contrast, consistent with no diurnal variation in glucose tolerance, obese subjects exhibited no decline in insulin sensitivity in the evening (AM 3.6 ± 0.7, PM 4.9 ± 1.0 × 10−5 min−1/pM). A marginally significant decline in (β-cell responsiveness was observed in the obese group (potentiation slope AM 388 ± 78, PM 233 ± 58 pM/mM, P < 0.05). Glucose tolerance is maintained when the pancreas adequately compensates for prevailing insulin resistance, a relationship described by the disposition index (SI, × Φ1). This product decreased 46% in nonobese subjects from morning to evening (P < 0.05), reflecting the inability of the pancreas to overcome prevailing insulin resistance, and resulting in evening glucose intolerance. No diurnal decline in the disposition index was observed in obese subjects. The diurnal rhythms in insulin sensitivity and secretion in nonobese subjects are not consistent with known rhythms in growth hormone or cortisol, but could be due to the effects of a putative diurnal rhythm of sympathetic activity, which would suppress both insulin sensitivity and secretion in the evening. The absence of a rhythm in the obese could reflect an autonomic or hormonal dysfunction that may be related to body-weight regulation.
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“In healthy nonobese individuals, SI is higher in the morning than 8 to 10 h later, in the late afternoon or early evening (29).”
From Circadian Misalignment Augments Markers of Insulin Resistance and Inflammation, Independently of Sleep Loss (2014) · cites this paper as [29]
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“This is consistent with previous studies that have shown that insulin sensitivity and glucose tolerance decreases progressively throughout the day with insulin sensitivity reaching a nadir in the evening (18,36,37).”
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Self-citationA Daily Rhythm in Glucose Tolerance
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“50 51 As a result, the ability to appropriately store and metabolise dietary glucose and lipid intake is progressively impaired throughout the day.”
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Peng, X., Fan, R., Xie, L., Shi, X., Dong, K., Zhang, S., Tao, J., Xu, W., Ma, D., Chen, J., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23010504 · Cited by 70
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BackgroundAder, M., Garvey, W. T., Phillips, L. S., Nemeroff, C. B., Gharabawi, G. M., Mahmoud, R. A., Greenspan, A. J., Berry, S. A., Musselman, D. L., Morein, J., et al. (2008) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2008.01.004 · Cited by 48
“First-phase insulin response (AIRG) was calculated as incremental insulin area from 0 to 10 min and glucose tolerance (KG) as the negative slope of the natural log of glucose versus time from 10 to 19 min (Lee et al., 1992).”
MethodSelf-citationFritz, J., Phillips, A., Hunt, L., Imam, A., Reid, K., Perreira, K., Mossavar-Rahmani, Y., Daviglus, M., Sotres-Alvarez, D., Zee, P., et al. (2020) · Sleep · doi:10.1093/sleep/zsaa218 · Cited by 36
Rovira‐Llopis, S., Luna-Marco, C., Perea‐Galera, L., Bañuls, C., Morillas, C., & Víctor, V. M. (2023) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-023-09853-x · Cited by 52
“…out that, compared to control lean subjects, people who have metabolic problems also develop alterations at the circadian cycle level in terms of the rhythmicity of metabolic processes, such as mitochondrial oxidative capacity [14], glucose homeostasis [15] and oxidation of substrates [14, 16].”
BackgroundPedrini, M. T., Niederwanger, A., Kranebitter, M., Tautermann, C., Ciardi, C., Tatarczyk, T., & Patsch, J. (2006) · Diabetologia · doi:10.1007/s00125-006-0262-z · Cited by 49
“In most studies, it has been observed that glucose tolerance is decreased in the afternoon or evening compared with the morning [37–39]; decreased glucose tolerance, in these studies, was shown to result from decreased insulin secretion [38–40], decreased insulin sensitivity [41, 42] or both [37, 43].”
BackgroundCircadian variation of the pancreatic islet transcriptome
Rakshit, K., Qian, J., Ernst, J., & Matveyenko, A. V. (2016) · Physiological Genomics · doi:10.1152/physiolgenomics.00019.2016 · Cited by 40
“Moreover, metabolic abnormalities associated with T2DM have also been shown to impair circadian control of insulin secretion (22).”
BackgroundEffects of aging on glucose regulation during wakefulness and sleep
Frank, S. A., Roland, D. C., Sturis, J., Byrne, M. M., Refetoff, S., Polonsky, K. S., & Cauter, E. V. (1995) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1995.269.6.e1006 · Cited by 38
Effect of meal sequence on postprandial lipid, glucose and insulin responses in young men
Burdge, G. C., Jones, A. E., Frye, S., Goodson, L., & Wootton, S. A. (2003) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1601722 · Cited by 40
Knutsson, A., Karlsson, B., Örnkloo, K., Landström, U., Lennernäs, M. A. ‐., & Eriksson, K. (2002) · Nutrition and Health · doi:10.1177/026010600201600207 · Cited by 36
Circadian regulation of cellular physiology
Peek, C. B., Ramsey, K. M., Levine, D. C., Marcheva, B., Perelis, M., & Bass, J. (2015) · Methods in Enzymology · doi:10.1016/bs.mie.2014.10.006 · Cited by 35
Scrimgeour, K., Gresham, M., Giles, L. R., Thomson, P. C., WYNN, P. C., & Newman, R. E. (2008) · Journal of Endocrinology · doi:10.1677/joe-07-0627 · Cited by 35
“For example, humans have a higher glucose output and insulin requirement in the early morning hours (Carroll & Nestel 1973, Lee et al. 1992), whereas rodents have higher concentrations of glucose and insulin in the dark period compared with the light period (Pauly & Scheving 1967), which may be…”
BackgroundInsulin resistance in healthy prepubertal twins.
Jefferies, C., Hofman, P., Knoblauch, H., Luft, F., Robinson, E., & Cutfield, W. (2004) · Jornal de Pediatria · doi:10.1016/j.jpeds.2004.01.059 · Cited by 36
An Endocrinologist's Guide to the Clock
Prasai, M., Pernicova, I., Grant, P. J., & SCOTT, E. M. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-2449 · Cited by 35
Predominantly night-time feeding and maternal glycaemic levels during pregnancy
Loy, S. L., Cheng, T. S., Colega, M., Cheung, Y. B., Godfrey, K. M., Gluckman, P. D., Kwek, K. Y. C., Saw, S., Chong, Y. S., Padmapriya, N., et al. (2016) · British Journal Of Nutrition · doi:10.1017/s0007114516000441 · Cited by 37
“It was suggested that the marked suppression of insulin sensitivity in the morning in obese subjects may lead to failure for detection with further reduction in insulin sensitivity((29)).”
BackgroundResultDiurnal Variations in Cardiovascular Function and Glucose Regulation in Normotensive Humans
Biston, P., Cauter, E. V., Ofek, G., Linkowski, P., Polonsky, K. S., & Degaute, J.-P. (1996) · Hypertension · doi:10.1161/01.hyp.28.5.863 · Cited by 35
The hypothalamic clock and its control of glucose homeostasis
Kalsbeek, A., Ruiter, M., la Fleur, S. E., Cailotto, C., Kreier, F., & Buijs, R. M. (2006) · Progress in brain research · doi:10.1016/s0079-6123(06)53017-1 · Cited by 33
Gyuk, P., Vassányi, I., & Kósa, I. (2019) · Journal of Healthcare Engineering · doi:10.1155/2019/8605206 · Cited by 29
“Both insulin sensitivity and secretion is supposed to change in the evening [33], but diabetics may also experience differences between early morning and afternoon hours.”
BackgroundWhat is bipolar disorder? A disease model of dysregulated energy expenditure
Mansur, R. B., Lee, Y. L., McIntyre, R. S., & Brietzke, E. M. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.04.006 · Cited by 33
Haldar, S., Egli, L., Castro, C. A. D., Tay, S. L., Koh, M. X. N., Darimont, C., Macé, K., & Henry, C. J. (2020) · BMJ Open Diabetes Research & Care · doi:10.1136/bmjdrc-2019-001099 · Cited by 34
The islet circadian clock: entrainment mechanisms, function and role in glucose homeostasis
Rakshit, K. P., Qian, J., Colwell, C. S., & Matveyenko, A. V. (2015) · Diabetes Obesity and Metabolism · doi:10.1111/dom.12523 · Cited by 36
“Finally, it is important to note that circadian rhythms in insulin secretion are disrupted in states associated with metabolic disease such as obesity and T2DM [30,33], implying an intriguing possibility that loss of circadian rhythmicity in insulin secretion may serve as an early biomarker of β-cell dysfunction in T2…”
BackgroundAlteration of postprandial glucose and insulin concentrations with meal frequency and composition
Kanaley, J. A., Heden, T. D., Liu, Y., & Fairchild, T. J. (2014) · British Journal Of Nutrition · doi:10.1017/s0007114514002128 · Cited by 31
“However, in obese subjects, this circadian variation is believed to be absent((29)), which is supported by our data.”
Metadata
- Authors
- Lee, A., Ader, M., Bray, G. A., & Bergman, R. N.
- Affiliations
- Pennington Biomedical Research Center (US)
- Venue
- Diabetes
- Publisher
- American Diabetes Association
- Published
- 1992-06-01
- Volume
- 41
- Issue
- 6
- Pages
- 750-759
- ISSN
- 0012-1797 (ISSN-L)
- 1939-327X
- OpenAlex
- W2025050665
- Cited by
- 193
- References
- 0
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 11 · 2023: 9 · 2022: 10 · 2021: 6 · 2020: 8 · 2019: 8 · 2018: 6 · 2017: 9 · 2016: 8 · 2015: 9 · 2014: 10 · 2013: 8 · 2012: 7
- FWCI
- 4.89
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Diabetes (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK029867, DK27619, DK29867)
- National Center for Research Resources (RR00425, M01RR000425)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Pancreatic function and diabetes
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
- Keywords
- diurnal variation, glucose tolerance, insulin sensitivity, insulin secretion, obesity, glucose effectiveness, first-phase insulin response, circadian rhythm, glucose tolerance test, insulin sensitivity index
- MeSH terms
- Insulin Secretion, Adult, Arginine, Body Weight, Circadian Rhythm, Female, Glucose Tolerance Test, Humans, Insulin, Male, Obesity, Reference Values, Tolbutamide, Body Mass Index
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