Association of the Composite Inflammatory Biomarker GlycA, with Exercise-Induced Changes in Body Habitus in Men and Women with Prediabetes

David B Bartlett, Cris A Slentz, Margery A Connelly, Lucy W Piner, Leslie H Willis, Lori A Bateman, Esther O Granville, Connie W Bales, Kim M Huffman, William E Kraus, David B Bartlett, Cris A Slentz, Margery A Connelly, Lucy W Piner, Leslie H Willis, Lori A Bateman, Esther O Granville, Connie W Bales, Kim M Huffman, William E Kraus

Abstract

GlycA is a new composite measure of systemic inflammation and a predictor of many inflammatory diseases. GlycA is the nuclear magnetic resonance spectroscopy-derived signal arising from glucosamine residues on acute-phase proteins. This study aimed to evaluate how exercise-based lifestyle interventions modulate GlycA in persons at risk for type 2 diabetes. GlycA, fitness, and body habitus were measured in 169 sedentary adults (45-75 years) with prediabetes randomly assigned to one of four six-month exercise-based lifestyle interventions. Interventions included exercise prescription based on the amount (energy expenditure (kcal/kg weight/week (KKW)) and intensity (%VO2peak). The groups were (1) low-amount/moderate-intensity (10KKW/50%) exercise; (2) high-amount/moderate-intensity (16KKW/50%) exercise; (3) high-amount/vigorous-intensity (16KKW/75%) exercise; and (4) a Clinical Lifestyle (combined diet plus low-amount/moderate-intensity exercise) intervention. Six months of exercise training and/or diet-reduced GlycA (mean Δ: -6.8 ± 29.2 μmol/L; p = 0.006) and increased VO2peak (mean Δ: 1.98 ± 2.6 mL/kg/min; p < 0.001). Further, visceral (mean Δ: -21.1 ± 36.6 cm2) and subcutaneous fat (mean Δ: -24.3 ± 41.0 cm2) were reduced, while liver density (mean Δ: +2.3 ± 6.5HU) increased, all p < 0.001. When including individuals in all four interventions, GlycA reductions were associated with reductions in visceral adiposity (p < 0.03). Exercise-based lifestyle interventions reduced GlycA concentrations through mechanisms related to exercise-induced modulations of visceral adiposity. This trial is registered with Clinical Trial Registration Number NCT00962962.

Figures

Figure 1
Figure 1
Mean (SEM) change scores for VO2peak (a), liver density (b), subcutaneous (c) and visceral adiposity (d), fasting glucose (e), and insulin (f) for each intervention. ∗∗p < 0.01 different from the High-Vig group; ψp < 0.05; ψψp < 0.01; ψψψp < 0.001 different from Clinical Lifestyle.
Figure 2
Figure 2
Mean (SEM) change scores for GlycA. Although there was a significant effect for time (p = 0.006) with an overall 2% reduction in GlycA, no differences were observed between groups (p > 0.05).

References

    1. Knowler W. C., Barrett-Connor E., Fowler S. E., et al. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. The New England Journal of Medicine. 2002;346(6):393–403. doi: 10.1056/NEJMoa012512.
    1. Li G., Zhang P., Wang J., et al. The long-term effect of lifestyle interventions to prevent diabetes in the China Da Qing Diabetes Prevention Study: a 20-year follow-up study. Lancet. 2008;371(9626):1783–1789. doi: 10.1016/S0140-6736(08)60766-7.
    1. Tuomilehto J. Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. The New England Journal of Medicine. 2001;344(18):1343–1350. doi: 10.1056/NEJM200105033441801.
    1. Pan X. R., Li G. W., Hu Y. H., et al. Effects of diet and exercise in preventing NIDDM in people with impaired glucose tolerance. The Da Qing IGT and Diabetes Study. Diabetes Care. 1997;20(4):537–544. doi: 10.2337/diacare.20.4.537.
    1. Kraus W. E., Houmard J. A., Duscha B. D., et al. Effects of the amount and intensity of exercise on plasma lipoproteins. The New England Journal of Medicine. 2002;347(19):1483–1492. doi: 10.1056/NEJMoa020194.
    1. Johnson J. L., Slentz C. A., Houmard J. A., et al. Exercise training amount and intensity effects on metabolic syndrome (from studies of a targeted risk reduction intervention through defined exercise) The American Journal of Cardiology. 2007;100(12):1759–1766. doi: 10.1016/j.amjcard.2007.07.027.
    1. Bateman L. A., Slentz C. A., Willis L. H., et al. Comparison of aerobic versus resistance exercise training effects on metabolic syndrome (from the Studies of a Targeted Risk Reduction Intervention Through Defined Exercise - STRRIDE-AT/RT) The American Journal of Cardiology. 2011;108(6):838–844. doi: 10.1016/j.amjcard.2011.04.037.
    1. Huffman K. M., Slentz C. A., Bateman L. A., et al. Exercise-induced changes in metabolic intermediates, hormones, and inflammatory markers associated with improvements in insulin sensitivity. Diabetes Care. 2011;34(1):174–176. doi: 10.2337/dc10-0709.
    1. Slentz C. A., Bateman L. A., Willis L. H., et al. Effects of exercise training alone vs a combined exercise and nutritional lifestyle intervention on glucose homeostasis in prediabetic individuals: a randomised trial. Diabetiologia. 2016;59(10):2088–2098. doi: 10.1007/s00125-016-4051-z.
    1. Gleeson M., Bishop N. C., Stensel D. J., Lindley M. R., Mastana S. S., Nimmo M. A. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nature Reviews. Immunology. 2011;11(9):607–615. doi: 10.1038/nri3041.
    1. Walsh N. P., Gleeson M., Shephard R. J., et al. Position statement. Part one: Immune function and exercise. Exercise Immunology Review. 2011;17(17):6–63.
    1. Cesari M., Penninx B. W., Newman A. B., et al. Inflammatory markers and onset of cardiovascular events: results from the Health ABC study. Circulation. 2003;108(19):2317–2322. doi: 10.1161/01.CIR.0000097109.90783.FC.
    1. Hammett C. J., Oxenham H. C., Baldi J. C., et al. Effect of six months’ exercise training on C-reactive protein levels in healthy elderly subjects. Journal of the American College of Cardiology. 2004;44(12):2411–2413. doi: 10.1016/j.jacc.2004.09.030.
    1. Tzoulaki I., Murray G. D., Lee A. J., Rumley A., Lowe G. D., Fowkes F. G. C-reactive protein, interleukin-6, and soluble adhesion molecules as predictors of progressive peripheral atherosclerosis in the general population: Edinburgh Artery Study. Circulation. 2005;112(7):976–983. doi: 10.1161/CIRCULATIONAHA.104.513085.
    1. Nishimoto N. Cytokine signal regulation and autoimmune disorders. Autoimmunity. 2005;38(5):359–367. doi: 10.1080/08916930500124106.
    1. Huffman K. M., Samsa G. P., Slentz C. A., et al. Response of high-sensitivity C-reactive protein to exercise training in an at-risk population. American Heart Journal. 2006;152(4):793–800. doi: 10.1016/j.ahj.2006.04.019.
    1. Ahmad T., Fiuzat M., Mark D. B., et al. The effects of exercise on cardiovascular biomarkers in patients with chronic heart failure. American Heart Journal. 2014;167(2):193–202. doi: 10.1016/j.ahj.2013.10.018. e1.
    1. Nicklas B. J., Hsu F. C., Brinkley T. J., et al. Exercise training and plasma C-reactive protein and interleukin-6 in elderly people. Journal of the American Geriatrics Society. 2008;56(11):2045–2052. doi: 10.1111/j.1532-5415.2008.01994.x.
    1. Bell J. D., Brown J. C., Nicholson J. K., Sadler P. J. Assignment of resonances for ‘acute-phase’ glycoproteins in high resolution proton NMR spectra of human blood plasma. FEBS Letters. 1987;215(2):311–315. doi: 10.1016/0014-5793(87)80168-0.
    1. Otvos J. D., Shalaurova I., Wolak-Dinsmore J., et al. GlycA: a composite nuclear magnetic resonance biomarker of systemic inflammation. Clinical Chemistry. 2015;61(5):714–723. doi: 10.1373/clinchem.2014.232918.
    1. Dungan K., Binkley P., Osei K. GlycA is a novel marker of inflammation among non-critically ill hospitalized patients with type 2 diabetes. Inflammation. 2015;38(3):1357–1363. doi: 10.1007/s10753-014-0107-8.
    1. Connelly M. A., Shimizu C., Winegar D. A., et al. Differences in GlycA and lipoprotein particle parameters may help distinguish acute Kawasaki disease from other febrile illnesses in children. BMC Pediatrics. 2016;16(1):p. 151. doi: 10.1186/s12887-016-0688-5.
    1. Dullaart R. P., Gruppen E. G., Connelly M. A., Otvos J. D., Lefrandt J. D. GlycA, a biomarker of inflammatory glycoproteins, is more closely related to the leptin/adiponectin ratio than to glucose tolerance status. Clinical Biochemistry. 2015;48(12):811–814. doi: 10.1016/j.clinbiochem.2015.05.001.
    1. Lorenzo C., Festa A., Hanley A. J., Rewers M. J., Escalante A., Haffner S. M. Novel protein glycan-derived markers of systemic inflammation and C-reactive protein in relation to glycemia, insulin resistance, and insulin secretion. Diabetes Care. 2017;40(3):375–382. doi: 10.2337/dc16-1569.
    1. Connelly M. A., Gruppen E. G., Otvos J. D., Dullaart R. P. Inflammatory glycoproteins in cardiometabolic disorders, autoimmune diseases and cancer. Clinica Chimica Acta. 2016;459:177–186. doi: 10.1016/j.cca.2016.06.012.
    1. McGarrah R. W., Kelly J. P., Craig D. M., et al. A novel protein glycan-derived inflammation biomarker independently predicts cardiovascular disease and modifies the association of HDL subclasses with mortality. Clinical Chemistry. 2017;63(1):288–296. doi: 10.1373/clinchem.2016.261636.
    1. Akinkuolie A. O., Buring J. E., Ridker P. M., Mora S. A novel protein glycan biomarker and future cardiovascular disease events. Journal of the American Heart Association. 2014;3(5, article e001221) doi: 10.1161/JAHA.114.001221.
    1. Gruppen E. G., Riphagen I. J., Connelly M. A., Otvos J. D., Bakker S. J., Dullaart R. P. GlycA, a pro-inflammatory glycoprotein biomarker, and incident cardiovascular disease: relationship with C-reactive protein and renal function. PloS One. 2015;10(9, article e0139057) doi: 10.1371/journal.pone.0139057.
    1. Duprez D. A., Otvos J., Sanchez O. A., Mackey R. H., Tracy R., Jacobs D. R., Jr Comparison of the predictive value of GlycA and other biomarkers of inflammation for total death, incident cardiovascular events, noncardiovascular and noncancer inflammatory-related events, and total cancer events. Clinical Chemistry. 2016;62(7):1020–1031. doi: 10.1373/clinchem.2016.255828.
    1. Akinkuolie A. O., Glynn R. J., Padmanabhan L., Ridker P. M., Mora S. Circulating N-linked glycoprotein side-chain biomarker, rosuvastatin therapy, and incident cardiovascular disease: an analysis from the JUPITER trial. Journal of the American Heart Association. 2016;5(7, article e003822) doi: 10.1161/JAHA.116.003822.
    1. Akinkuolie A. O., Pradhan A. D., Buring J. E., Ridker P. M., Mora S. Novel protein glycan side-chain biomarker and risk of incident type 2 diabetes mellitus. Arteriosclerosis, Thrombosis, and Vascular Biology. 2015;35(6):1544–1550. doi: 10.1161/ATVBAHA.115.305635.
    1. Connelly M. A., Gruppen E. G., Wolak-Dinsmore J., et al. GlycA, a marker of acute phase glycoproteins, and the risk of incident type 2 diabetes mellitus: PREVEND study. Clinica Chimica Acta. 2016;452:10–17. doi: 10.1016/j.cca.2015.11.001.
    1. Ormseth M. J., Chung C. P., Oeser A. M., et al. Utility of a novel inflammatory marker, GlycA, for assessment of rheumatoid arthritis disease activity and coronary atherosclerosis. Arthritis Research & Therapy. 2015;17(1):p. 117. doi: 10.1186/s13075-015-0646-x.
    1. Bartlett D. B., Connelly M. A., AbouAssi H., et al. A novel inflammatory biomarker, GlycA, associates with disease activity in rheumatoid arthritis and cardio-metabolic risk in BMI-matched controls. Arthritis Research & Therapy. 2016;18(1):p. 86. doi: 10.1186/s13075-016-0982-5.
    1. Chung C. P., Ormseth M. J., Connelly M. A., et al. GlycA, a novel marker of inflammation, is elevated in systemic lupus erythematosus. Lupus. 2016;25(3):296–300. doi: 10.1177/0961203315617842.
    1. Durcan L., Winegar D. A., Connelly M. A., Otvos J. D., Magder L. S., Petri M. Longitudinal evaluation of lipoprotein variables in systemic lupus erythematosus reveals adverse changes with disease activity and prednisone and more favorable profiles with hydroxychloroquine therapy. The Journal of Rheumatology. 2016;43(4):745–750. doi: 10.3899/jrheum.150437.
    1. Joshi A. A., Lerman J. B., Aberra T. M., et al. GlycA is a novel biomarker of inflammation and subclinical cardiovascular disease in psoriasis. Circulation Research. 2016;119(11):1242–1253. doi: 10.1161/CIRCRESAHA.116.309637.
    1. Howley E. T. Type of activity: resistance, aerobic and leisure versus occupational physical activity. Medicine and Science in Sports and Exercise. 2001;33(6 Supplement):S364–S369. doi: 10.1097/00005768-200106001-00005. discussion S419-20.
    1. Kraus W. E., Torgan C. E., Duscha B. D., et al. Studies of a targeted risk reduction intervention through defined exercise (STRRIDE) Medicine and Science in Sports and Exercise. 2001;33(10):1774–1784. doi: 10.1097/00005768-200110000-00025.
    1. Siri W. E. Body composition from fluid spaces and density: analysis of methods. 1961. Nutrition. 1993;9(5):480–491. discussion 480, 492.
    1. Ginde S. R., Geliebter A., Rubiano F., et al. Air displacement plethysmography: validation in overweight and obese subjects. Obesity Research. 2005;13(7)(7):p. 1232. doi: 10.1038/oby.2005.146.
    1. Dempster P., Aitkens S. A new air displacement method for the determination of human body composition. Medicine and Science in Sports and Exercise. 1995;27(12):1692–1697.
    1. Irving B. A., Weltman J. Y., Brock D. W., Davis C. K., Gaesser G. A., Weltman A. NIH ImageJ and Slice-O-Matic computed tomography imaging software to quantify soft tissue. Obesity (Silver Spring) 2007;15(2):370–376. doi: 10.1038/oby.2007.573.
    1. Ellis K. J. Human body composition: in vivo methods. Physiological Reviews. 2000;80(2):649–680.
    1. Jeyarajah E. J., Cromwell W. C., Otvos J. D. Lipoprotein particle analysis by nuclear magnetic resonance spectroscopy. Clinics in Laboratory Medicine. 2006;26(4):847–870. doi: 10.1016/j.cll.2006.07.006.
    1. Faul F., Erdfelder E., Lang A. G., Buchner A. G∗Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods. 2007;39(2):175–191. doi: 10.3758/BF03193146.
    1. Gabay C., Kushner I. Acute-phase proteins and other systemic responses to inflammation. The New England Journal of Medicine. 1999;340(6):448–454. doi: 10.1056/NEJM199902113400607.
    1. Gornik O., Lauc G. Glycosylation of serum proteins in inflammatory diseases. Disease Markers. 2008;25(4-5):267–278. doi: 10.1155/2008/493289.
    1. Kremer J. M., Wilting J., Janssen L. H. Drug binding to human alpha-1-acid glycoprotein in health and disease. Pharmacological Reviews. 1988;40(1):1–47.
    1. Arnold J. N., Saldova R., Hamid U. M., Rudd P. M. Evaluation of the serum N-linked glycome for the diagnosis of cancer and chronic inflammation. Proteomics. 2008;8(16):3284–3293. doi: 10.1002/pmic.200800163.
    1. Marino K., Bones J., Kattla J. J., Rudd P. M. A systematic approach to protein glycosylation analysis: a path through the maze. Nature Chemical Biology. 2010;6(10):713–723. doi: 10.1038/nchembio.437.
    1. Gornik O., Royle L., Harvey D. J., et al. Changes of serum glycans during sepsis and acute pancreatitis. Glycobiology. 2007;17(12):1321–1332. doi: 10.1093/glycob/cwm106.
    1. Higai K., Azuma Y., Aoki Y., Matsumoto K. Altered glycosylation of α1-acid glycoprotein in patients with inflammation and diabetes mellitus. Clinica Chimica Acta. 2003;329(1-2):117–125. doi: 10.1016/S0009-8981(02)00427-8.
    1. Bleasby A. J., Knowles J. C., Cooke N. J. Microheterogeneity of α1-acid glycoprotein: lack of discrimination between benign and malignant inflammatory disease of the lung. Clinica Chimica Acta. 1985;150(3):231–235. doi: 10.1016/0009-8981(85)90249-9.
    1. Fischer K., Kettunen J., Würtz P., et al. Biomarker profiling by nuclear magnetic resonance spectroscopy for the prediction of all-cause mortality: an observational study of 17,345 persons. PLoS Medicine. 2014;11(2, article e1001606) doi: 10.1371/journal.pmed.1001606.
    1. Prescott E., Hjardem-Hansen R., Dela F., Teisner A. S., Nielsen H. Exercise training in older patients with systolic heart failure: adherence, exercise capacity, inflammation and glycemic control. Scandinavian Cardiovascular Journal. 2009;43(4):249–255. doi: 10.1080/14017430802593427.
    1. Lavoie M. E., Faraj M., Strychar I., et al. Synergistic associations of physical activity and diet quality on cardiometabolic risk factors in overweight and obese postmenopausal women. The British Journal of Nutrition. 2013;109(4):605–614. doi: 10.1017/S0007114512001699.
    1. Finucane F. M., Luan J., Wareham N. J., et al. Savage D. B. Correlation of the leptin:adiponectin ratio with measures of insulin resistance in non-diabetic individuals. Diabetologia. 2009;52(11):2345–2349. doi: 10.1007/s00125-009-1508-3.
    1. Gastaldelli A., Miyazaki Y., Pettiti M., et al. Metabolic effects of visceral fat accumulation in type 2 diabetes. The Journal of Clinical Endocrinology and Metabolism. 2002;87(11):5098–5103. doi: 10.1210/jc.2002-020696.
    1. Tilg H., Moschen A. R. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nature Reviews. Immunology. 2006;6(10):772–783. doi: 10.1038/nri1937.
    1. Chandler P. D., Akinkuolie A. O., Tobias D. K., et al. Association of N-linked glycoprotein acetyls and colorectal cancer incidence and mortality. PloS One. 2016;11(11, article e0165615) doi: 10.1371/journal.pone.0165615.
    1. Duscha B. D., Slentz C. A., Johnson J. L., et al. Effects of exercise training amount and intensity on peak oxygen consumption in middle-age men and women at risk for cardiovascular disease. Chest. 2005;128(4):2788–2793. doi: 10.1378/chest.128.4.2788.
    1. Slentz C. A., Aiken L. B., Houmard J. A., et al. Inactivity, exercise, and visceral fat. STRRIDE: a randomized, controlled study of exercise intensity and amount. Journal of Applied Physiology. 2005;99(4):1613–1618. doi: 10.1152/japplphysiol.00124.2005.
    1. Karstoft K., Solomon T. P., Laye M. J., Pedersen B. K. Daily marathon running for a week—the biochemical and body compositional effects of participation. Journal of Strength and Conditioning Research. 2013;27(11):2927–2933. doi: 10.1519/JSC.0b013e318289e39d.
    1. Boyum A., Wiik P., Gustavsson E., et al. The effect of strenuous exercise, calorie deficiency and sleep deprivation on white blood cells, plasma immunoglobulins and cytokines. Scandinavian Journal of Immunology. 1996;43(2):228–235. doi: 10.1046/j.1365-3083.1996.d01-32.x.
    1. Liesen H., Dufaux B., Hollmann W. Modifications of serum glycoproteins the days following a prolonged physical exercise and the influence of physical training. European Journal of Applied Physiology and Occupational Physiology. 1977;37(4):243–254. doi: 10.1007/BF00430954.
    1. Gilmore I. T., Burroughs A., Murray-Lyon I. M., Williams R., Jenkins D., Hopkins A. Indications, methods, and outcomes of percutaneous liver biopsy in England and Wales: an audit by the British Society of Gastroenterology and the Royal College of Physicians of London. Gut. 1995;36(3):437–441. doi: 10.1136/gut.36.3.437.
    1. Banerji M. A., Buckley M. C., Chaiken R. L., Gordon D., Lebovitz H. E., Kral J. G. Liver fat, serum triglycerides and visceral adipose tissue in insulin-sensitive and insulin-resistant black men with NIDDM. International Journal of Obesity and Related Metabolic Disorders. 1995;19(12):846–850.
    1. Goto T., Onuma T., Takebe K., Kral J. G. The influence of fatty liver on insulin clearance and insulin resistance in non-diabetic Japanese subjects. International Journal of Obesity and Related Metabolic Disorders. 1995;19(12):841–845.
    1. Saadeh S., Younossi Z. M., Remer E. M., et al. The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology. 2002;123(3):745–750. doi: 10.1053/gast.2002.35354.
    1. Ricci C., Longo R., Gioulis E., et al. Noninvasive in vivo quantitative assessment of fat content in human liver. Journal of Hepatology. 1997;27(1):108–113. doi: 10.1016/S0168-8278(97)80288-7.
    1. Kolak M., Westerbacka J., Velagapudi V. R., et al. Adipose tissue inflammation and increased ceramide content characterize subjects with high liver fat content independent of obesity. Diabetes. 2007;56(8)(8):p. 1960. doi: 10.2337/db07-0111.
    1. Seppala-Lindroos A., Vehkavaara S., Häkkinen A. M., et al. Fat accumulation in the liver is associated with defects in insulin suppression of glucose production and serum free fatty acids independent of obesity in normal men. The Journal of Clinical Endocrinology and Metabolism. 2002;87(7):3023–3028. doi: 10.1210/jcem.87.7.8638.
    1. Fabbrini E., Magkos F. Hepatic steatosis as a marker of metabolic dysfunction. Nutrients. 2015;7(6):4995–5019. doi: 10.3390/nu7064995.
    1. Slentz C. A., Bateman L. A., Willis L. H., et al. Effects of aerobic vs. resistance training on visceral and liver fat stores, liver enzymes, and insulin resistance by HOMA in overweight adults from STRRIDE AT/RT. American Journal of Physiology. Endocrinology and Metabolism. 2011;301(5):E1033–E1039. doi: 10.1152/ajpendo.00291.2011.
    1. Vozarova B., Stefan N., Lindsay R. S., et al. High alanine aminotransferase is associated with decreased hepatic insulin sensitivity and predicts the development of type 2 diabetes. Diabetes. 2002;51(6):1889–1895. doi: 10.2337/diabetes.51.6.1889.
    1. Davidson L. E., Kuk J. L., Church T. S., Ross R. Protocol for measurement of liver fat by computed tomography. Journal of Applied Physiology. 2006;100(3):864–868. doi: 10.1152/japplphysiol.00986.2005.
    1. Kreel L. Computerised tomography and the liver. Clinical Radiology. 1977;28(6):571–581. doi: 10.1016/S0009-9260(77)80031-7.
    1. Gonzalez J. T., Fuchs C. J., Betts J. A., van Loon L. J. Liver glycogen metabolism during and after prolonged endurance-type exercise. American Journal of Physiology. Endocrinology and Metabolism. 2016;311(3):E543–E553. doi: 10.1152/ajpendo.00232.2016.
    1. Gonzalez J. T., Fuchs C. J., Smith F. E., et al. Ingestion of glucose or sucrose prevents liver but not muscle glycogen depletion during prolonged endurance-type exercise in trained cyclists. American Journal of Physiology. Endocrinology and Metabolism. 2015;309(12):E1032–E1039. doi: 10.1152/ajpendo.00376.2015.
    1. Macauley M., Smith F. E., Thelwall P. E., Hollingsworth K. G., Taylor R. Diurnal variation in skeletal muscle and liver glycogen in humans with normal health and type 2 diabetes. Clinical Science (London, England) 2015;128(10):707–713. doi: 10.1042/CS20140681.
    1. Stevenson E. J., Thelwall P. E., Thomas K., Smith F., Brand-Miller J., Trenell M. I. Dietary glycemic index influences lipid oxidation but not muscle or liver glycogen oxidation during exercise. American Journal of Physiology. Endocrinology and Metabolism. 2009;296(5):E1140–E1147. doi: 10.1152/ajpendo.90788.2008.

Source: PubMed

Sponsors et collaborateurs

Les conditions médicales

Interventions en matière de drogue

3
S'abonner