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Effects of acute intermittent hypoxia on glucose metabolism in awake healthy volunteers.
Open accessAbstract
Accumulating evidence suggests that obstructive sleep apnea is associated with alterations in glucose metabolism. Although the pathophysiology of metabolic dysfunction in obstructive sleep apnea is not well understood, studies of murine models indicate that intermittent hypoxemia has an important contribution. However, corroborating data on the metabolic effects of intermittent hypoxia on glucose metabolism in humans are not available. Thus the primary aim of this study was to characterize the acute effects of intermittent hypoxia on glucose metabolism. Thirteen healthy volunteers were subjected to 5 h of intermittent hypoxia or normoxia during wakefulness in a randomized order on two separate days. The intravenous glucose tolerance test (IVGTT) was used to assess insulin-dependent and insulin-independent measures of glucose disposal. The IVGTT data were analyzed using the minimal model to determine insulin sensitivity (S I ) and glucose effectiveness (S G ). Drops in oxyhemoglobin saturation were induced during wakefulness at an average rate of 24.3 events/h. Compared with the normoxia condition, intermittent hypoxia was associated with a decrease in S I [4.1 vs. 3.4 (mU/l) −1 ·min −1 ; P = 0.0179] and S G (1.9 vs. 1.3 min −1 ×10 −2 , P = 0.0065). Despite worsening insulin sensitivity with intermittent hypoxia, pancreatic insulin secretion was comparable between the two conditions. Heart rate variability analysis showed the intermittent hypoxia was associated with a shift in sympathovagal balance toward an increase in sympathetic nervous system activity. The average R-R interval on the electrocardiogram was 919.0 ms during the normoxia condition and 874.4 ms during the intermittent hypoxia condition ( P < 0.04). Serum cortisol levels after intermittent hypoxia and normoxia were similar. Hypoxic stress in obstructive sleep apnea may increase the predisposition for metabolic dysfunction by impairing insulin sensitivity, glucose effectiveness, and insulin secretion.
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“One week with 5.7 h TIB compared to 8.5 h TIB affected the genes associated with circadian rhythms (PER1, PER2, PER3, CRY2, CLOCK, NR1D1, NR1D2, RORA, DEC1, CSNK1E), sleep homeostasis (IL-6, STAT3, KCNV2, CAMK2D), oxidative stress (PRDX2, PRDX5), and metabolism (SLC2A5, GHRL, ABCA1), as assessed by transcriptome analysis [42]*.”
From Metabolic effects of sleep disruption, links to obesity and diabetes (2014) · cites this paper as [42]
Citations
Cites
Heart Rate Variability: Standards of Measurement, Physiological Interpretation, and Clinical Use
Electrophysiology, T. F. O. T. E. S. O. C. T. N. A. (1996) · Circulation · doi:10.1161/01.cir.93.5.1043 · Cited by 17,159
Heart rate variability: Standards of measurement, physiological interpretation, and clinical use
Malik, M., Bigger, J. T., Camm, A. J., Kleiger, R. E., Malliani, A., Moss, A. J., & Schwartz, P. J. (1996) · European Heart Journal · doi:10.1093/oxfordjournals.eurheartj.a014868 · Cited by 15,289
Global Burden of Diabetes, 1995–2025: Prevalence, numerical estimates, and projections
King, H. O. M., Aubert, R. E., & Herman, W. H. (1998) · Diabetes Care · doi:10.2337/diacare.21.9.1414 · Cited by 6,294
C-Reactive Protein, Interleukin 6, and Risk of Developing Type 2 Diabetes Mellitus
Pradhan, A. D. (2001) · JAMA · doi:10.1001/jama.286.3.327 · Cited by 4,433
Type 2 diabetes: principles of pathogenesis and therapy
Stumvoll, M., Goldstein, B. J., & van Haeften, T. W. (2005) · The Lancet · doi:10.1016/s0140-6736(05)61032-x · Cited by 2,662
Kahn, S. E. (2003) · Diabetologia · doi:10.1007/s00125-002-1009-0 · Cited by 2,166
Quantitative estimation of insulin sensitivity.
Bergman, R. N., Ider, Y. Z., Bowden, C. R., & Cobelli, C. (1979) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1979.236.6.e667 · Cited by 1,874 · cited 2×
“The resulting glucose and insulin values during the intermittent hypoxia and normoxia conditions were subjected to the minimal model analysis (5, 7, 9) for determination of insulin sensitivity (SI), glucose effectiveness (SG), and glucose effectiveness at zero insulin (GEZI).”
MethodKahn, S. E., Prigeon, R. L., McCulloch, D. K., Boyko, E. J., Bergman, R. N., Schwartz, M. W., Neifing, J. L., Ward, W. K., Beard, J. C., & Palmer, J. P. (1993) · Diabetes · doi:10.2337/diab.42.11.1663 · Cited by 1,405
Punjabi, N. M. (2004) · American Journal of Epidemiology · doi:10.1093/aje/kwh261 · Cited by 1,107
Self-citationAssessment of Insulin Sensitivityin Vivo*
Bergman, R. N., Finegood, D. T., & Ader, M. (1985) · Endocrine Reviews · doi:10.1210/edrv-6-1-45 · Cited by 1,072
Low-Grade Systemic Inflammation and the Development of Type 2 Diabetes
Duncan, B. B., Schmidt, M. I., Pankow, J. S., Ballantyne, C. M., Couper, D., Vigo, A., Hoogeveen, R., Folsom, A. R., & Heiss, G. (2003) · Diabetes · doi:10.2337/diabetes.52.7.1799 · Cited by 1,036
Association of Sleep Apnea and Type II Diabetes
Reichmuth, K. J., Austin, D., Skatrud, J. B., & Young, T. B. (2005) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200504-637oc · Cited by 787
Glucocorticoids and insulin resistance: old hormones, new targets
ANDREWS, R. C., & WALKER, B. R. (1999) · Clinical Science · doi:10.1042/cs0960513 · Cited by 731
Potential Role of TNF-α in the Pathogenesis of Insulin Resistance and Type 2 Diabetes
Moller, D. E. (2000) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(00)00272-1 · Cited by 730
Epinephrine-induced insulin resistance in man
Deibert, D. C., & Defronzo, R. A. (1980) · Journal of Clinical Investigation · doi:10.1172/jci109718 · Cited by 557 · cited 2×
“Indeed, administration of epinephrine to healthy volunteers decreases glycogenesis, increases glycolysis, and diminishes the ability of glucose to stimulate its own disposal (13, 23).”
BackgroundBoston, R., Stefanovski, D., Moate, P. J., Sumner, A. E., Watanabe, R. M., & Bergman, R. N. (2003) · Diabetes Technology & Therapeutics · doi:10.1089/152091503322641060 · Cited by 426
Lambillotte, C., Gilon, P., & Henquin, J. C. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119175 · Cited by 419
An Update on the Etiology and Epidemiology of Diabetes Mellitus
Adeghate, E. A., Schattner, P. L., & Dunn, E. V. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1372.029 · Cited by 389
Proposed mechanisms for the induction of insulin resistance by oxidative stress
Bloch-Damti, A., & Bashan, N. (2005) · Antioxidants & Redox Signaling · doi:10.1089/ars.2005.7.1553 · Cited by 388
Intermittent Hypoxia Increases Insulin Resistance in Genetically Obese Mice
Polotsky, V. Y., Li, J., Punjabi, N. M., Rubin, A. E., Smith, P. L., Schwartz, A. R., & O'Donnell, C. P. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.048173 · Cited by 386
Self-citationDisorders of glucose metabolism in sleep apnea
Punjabi, N. M., & Polotsky, V. Y. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00695.2005 · Cited by 381
Self-citationIntermittent Hypoxia Causes Insulin Resistance in Lean Mice Independent of Autonomic Activity
Iiyori, N., Alonso, L. C., Li, J., Sanders, M. H., Garcia-Ocana, A., O'Doherty, R. M., Polotsky, V. Y., & O'Donnell, C. P. (2007) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200610-1527oc · Cited by 373
Ali, M. K., Weber, M. B., & Narayan, K. M. V. (2010) · Wiley eBooks · doi:10.1002/9781444324808.ch5 · Cited by 316
Hypoxia Causes Glucose Intolerance in Humans
Oltmanns, K. M., Gehring, H., Rudolf, S., Schultes, B., Rook, S., Schweiger, U., Jan Born, A., Fehm, H. L., & Peters, A. (2004) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200308-1200oc · Cited by 217
Minimal Model: Perspective from 2005
Bergman, R. N. (2005) · Hormone Research in Paediatrics · doi:10.1159/000089312 · Cited by 216
The effect of altitude hypoxia on glucose homeostasis in men
Larsen, J. J., Hansen, J. M., Olsen, N. V., Galbo, H., & Dela, F. (1997) · The Journal of Physiology · doi:10.1111/j.1469-7793.1997.241bf.x · Cited by 206
Oxidative stress and impaired insulin secretion in type 2 diabetes
ROBERTSON, R. (2006) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2006.09.002 · Cited by 168
Acute noradrenergic activation induces insulin resistance in human skeletal muscle
Lembo, G., Capaldo, B., Rendina, V., Iaccarino, G., Napoli, R., Guida, R., Trimarco, B., & Sacca, L. (1994) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1994.266.2.e242 · Cited by 136
Yokoe, T., Alonso, L. C., Romano, L. C., Rosa, T. C., O'Doherty, R. M., García-Ocaña, A., Minoguchi, K., & O'Donnell, C. P. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.143586 · Cited by 125
Differences in Polysomnography Predictors for Hypertension and Impaired Glucose Tolerance
Sulit, L., Storfer‐Isser, A., Kirchner, H. L., & Redline, S. S. (2006) · SLEEP · doi:10.1093/sleep/29.6.777 · Cited by 115
Beard, J. C., Halter, J. B., Best, J. D., Pfeifer, M. A., & Porte, D. (1984) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1984.247.5.e592 · Cited by 109
Braun, B., Rock, P. B., Zamudio, S., Wolfel, G. E., Mazzeo, R. S., Muza, S. R., Fulco, C. S., MOORE, L. G., & Butterfield, G. E. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.91.2.623 · Cited by 101
Islet adaptation to insulin resistance: mechanisms and implications for intervention
Åhrén, B., & Pacini, G. (2004) · Diabetes Obesity and Metabolism · doi:10.1111/j.1463-1326.2004.00361.x · Cited by 86
Effect of Hypoxia on Blood Glucose, Hormones, and Insulin Receptor Functions in Newborn Calves
Cheng, N., Cai, W., Jiang, M., & Wu, S. (1997) · Pediatric Research · doi:10.1203/00006450-199706000-00009 · Cited by 77
Larsson, H., & Ahrén, B. (1999) · Diabetologia · doi:10.1007/s001250051251 · Cited by 73
Humpeler, E., Skrabal, F., & Bartsch, G. (1980) · European Journal of Applied Physiology · doi:10.1007/bf00421324 · Cited by 71
The Effect of Hypoxia on Plasma Leptin and Insulin in Newborn and Juvenile Rats
Raff, H., Bruder, E. D., & Jankowski, B. M. (1999) · Endocrine · doi:10.1385/endo:11:1:37 · Cited by 55
Effect of Neonatal Hypoxia on Leptin, Insulin, Growth Hormone and Body Composition in the Rat
Raff, H., Bruder, E. D., Jankowski, B. M., & Colman, R. J. (2001) · Hormone and Metabolic Research · doi:10.1055/s-2001-14929 · Cited by 54
Hypoxic alterations of cortisol circadian rhythm in man after simulation of a long duration flight
Coste, O., Beers, P. V., Bogdan, A., Charbuy, H., & Touitou, Y. (2005) · Steroids · doi:10.1016/j.steroids.2005.05.003 · Cited by 50
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Metadata
- Authors
- Louis, M., & Punjabi, N. M.
- Affiliations
- Johns Hopkins University (US)
- Venue
- Journal of Applied Physiology
- Publisher
- American Physiological Society
- Published
- 2009-05
- Volume
- 106
- Issue
- 5
- Pages
- 1538-1544
- ISSN
- 0161-7567 (ISSN-L)
- 8750-7587
- 1522-1601
- PMC
- PMC2681331
- OpenAlex
- W2153473929
- Cited by
- 342
- References
- 40
- Citations by year
- 2026: 9 · 2025: 13 · 2024: 14 · 2023: 11 · 2022: 14 · 2021: 20 · 2020: 17 · 2019: 17 · 2018: 28 · 2017: 24 · 2016: 30 · 2015: 29 · 2014: 26 · 2013: 28 · 2012: 23
- FWCI
- 13.74
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Applied Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute for Health and Care Research
- Institut National de la Santé et de la Recherche Médicale
- National Institutes of Health
- National Heart, Lung, and Blood Institute (HL-07578)
- National Center for Research Resources (UL1RR025005)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Obstructive Sleep Apnea Research
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and related disorders
- Keywords
- acute intermittent hypoxia, glucose metabolism, obstructive sleep apnea, insulin sensitivity, glucose effectiveness, insulin secretion, glucose tolerance, sympathovagal balance, heart rate variability, cortisol, hypoxic stress, metabolic dysfunction
- MeSH terms
- Insulin Secretion, Adolescent, Adult, Hypoxia, Blood Glucose, Electrocardiography, Glucose, Glucose Tolerance Test, Heart, Heart Rate, Humans, Insulin, Insulin Resistance, Oxyhemoglobins, Sympathetic Nervous System, Vagus Nerve, Sleep Apnea, Obstructive, Young Adult
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