Sedentary behaviour is a key determinant of metabolic inflexibility

Journal of Physiology

Volumn 596, Issue 8, 2018, Pages 1319-1330

  Rynders, Corey A ^a   Blanc, Stephane ^b,c   DeJong, Nathan ^a   Bessesen, Daniel H ^a,d   Bergouignan, Audrey ^a,b,c  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c CNRS   (France)

^d DENVER HEALTH MEDICAL CENTER   (United States)

Author keywords

glucose metabolism; insulin sensitivity; lipid metabolism; obesity; Physical activity; physical inactivity; weight regulation

Indexed keywords

AEROBIC EXERCISE; ARTICLE; BODY WEIGHT GAIN; EXPERIMENTAL STUDY; HUMAN; LIFESTYLE MODIFICATION; METABOLIC DISORDER; METABOLIC REGULATION; PHYSICAL ACTIVITY; PHYSICAL INACTIVITY; PREDICTION; PRIORITY JOURNAL; RISK FACTOR; SITTING; THERAPY EFFECT; ENERGY METABOLISM; EXERCISE; INSULIN RESISTANCE; LIPID METABOLISM;

ENERGY METABOLISM; EXERCISE; HUMANS; INSULIN RESISTANCE; LIPID METABOLISM; SEDENTARY BEHAVIOR;

EID: 85021700498     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP273282     Document Type: Article

References (67)

1. Altenburg TM, Rotteveel J, Serne EH & Chinapaw MJ (2016). Effects of multiple sedentary days on metabolic risk factors in free-living conditions: lessons learned and future recommendations. Front Physiol 7, 616.
2. Astrup A (2011). The relevance of increased fat oxidation for body-weight management: metabolic inflexibility in the predisposition to weight gain. Obes Rev 12, 859–865.
3. Bailey DP & Locke CD (2015). Breaking up prolonged sitting with light-intensity walking improves postprandial glycemia, but breaking up sitting with standing does not. J Sci Med Sport 18, 294–298.
4. Battaglia GM, Zheng D, Hickner RC & Houmard JA (2012). Effect of exercise training on metabolic flexibility in response to a high-fat diet in obese individuals. Am J Physiol Endocrinol Metab 303, E1440–E1445.
5. Bergouignan A, Antoun E, Momken I, Schoeller DA, Gauquelin-Koch G, Simon C & Blanc S (2013a). Effect of contrasted levels of habitual physical activity on metabolic flexibility. J Appl Physiol (1985) 114, 371–379.
6. Bergouignan A, Latouche C, Heywood S, Grace MS, Reddy-Luthmoodoo M, Natoli AK, Owen N, Dunstan DW & Kingwell BA (2016). Frequent interruptions of sedentary time modulates contraction- and insulin-stimulated glucose uptake pathways in muscle: Ancillary analysis from randomized clinical trials. Sci Rep 6, 32044.
7. Bergouignan A, Momken I, Lefai E, Antoun E, Schoeller DA, Platat C, Chery I, Zahariev A, Vidal H, Gabert L, Normand S, Freyssenet D, Laville M, Simon C & Blanc S (2013b). Activity energy expenditure is a major determinant of dietary fat oxidation and trafficking, but the deleterious effect of detraining is more marked than the beneficial effect of training at current recommendations. Am J Clin Nutr 98, 648–658.
8. Bergouignan A, Rudwill F, Simon C & Blanc S (2011). Physical inactivity as the culprit of metabolic inflexibility: evidence from bed-rest studies. J Appl Physiol 111, 1201–1210.
9. Bergouignan A, Schoeller DA, Normand S, Gauquelin-Koch G, Laville M, Shriver T, Desage M, Le Maho Y, Ohshima H, Gharib C & Blanc S (2006). Effect of physical inactivity on the oxidation of saturated and monounsaturated dietary fatty acids: results of a randomized trial. PLoS Clin Trials 1, e27.
10. Bergouignan A, Trudel G, Simon C, Chopard A, Schoeller DA, Momken I, Votruba SB, Desage M, Burdge GC, Gauquelin-Koch G, Normand S & Blanc S (2009). Physical inactivity differentially alters dietary oleate and palmitate trafficking. Diabetes 58, 367–376.
11. Blanc S, Normand S, Pachiaudi C, Duvareille M & Gharib C (2000a). Leptin responses to physical inactivity induced by simulated weightlessness. Am J Physiol Regul Integr Comp Physiol 279, R891–R898.
12. Blanc S, Normand S, Pachiaudi C, Fortrat JO, Laville M & Gharib C (2000b). Fuel homeostasis during physical inactivity induced by bed rest. J Clin Endocrinol Metab 85, 2223–2233.
13. Blanc S, Normand S, Ritz P, Pachiaudi C, Vico L, Gharib C & Gauquelin-Koch G (1998). Energy and water metabolism, body composition, and hormonal changes induced by 42 days of enforced inactivity and simulated weightlessness. J Clin Endocrinol Metab 83, 4289–4297.
14. Blankenship JM, Granados K & Braun B (2014). Effects of subtracting sitting versus adding exercise on glycemic control and variability in sedentary office workers. Appl Physiol Nutr Metab 39, 1286–1293.
15. Bouchard C, Blair SN & Katzmarzyk PT (2015). Less sitting, more physical activity, or higher fitness? Mayo Clin Proc 90, 1533–1540.
16. Boyle KE, Zheng D, Anderson EJ, Neufer PD & Houmard JA (2012). Mitochondrial lipid oxidation is impaired in cultured myotubes from obese humans. Int J Obes (Lond) 36, 1025–1031.
17. Bruce CR, Thrush AB, Mertz VA, Bezaire V, Chabowski A, Heigenhauser GJ & Dyck DJ (2006). Endurance training in obese humans improves glucose tolerance and mitochondrial fatty acid oxidation and alters muscle lipid content. Am J Physiol Endocrinol Metab 291, E99–E107.
18. Buckley JP, Mellor DD, Morris M & Joseph F (2014). Standing-based office work shows encouraging signs of attenuating post-prandial glycaemic excursion. Occup Environ Med 71, 109–111.
19. Calles-Escandon J, Goran MI, O'Connell M, Nair KS & Danforth E Jr (1996). Exercise increases fat oxidation at rest unrelated to changes in energy balance or lipolysis. Am J Physiol Endocrinol Metab 270, E1009–E1014.
20. Corpeleijn E, Mensink M, Kooi ME, Roekaerts PM, Saris WH & Blaak EE (2008). Impaired skeletal muscle substrate oxidation in glucose-intolerant men improves after weight loss. Obesity (Silver Spring) 16, 1025–1032.
21. Dempsey PC, Blankenship JM, Larsen RN, Sacre JW, Sethi P, Straznicky NE, Cohen ND, Cerin E, Lambert GW, Owen N, Kingwell BA & Dunstan DW (2017). Interrupting prolonged sitting in type 2 diabetes: nocturnal persistence of improved glycaemic control. Diabetologia 60, 499–507.
22. Dempsey PC, Larsen RN, Sethi P, Sacre JW, Straznicky NE, Cohen ND, Cerin E, Lambert GW, Owen N, Kingwell BA & Dunstan DW (2016). Benefits for type 2 diabetes of interrupting prolonged sitting with brief bouts of light walking or simple resistance activities. Diabetes Care 39, 964–972.
23. Dirks ML, Wall BT, van de Valk B, Holloway TM, Holloway GP, Chabowski A, Goossens GH & van Loon LJ (2016). One week of bed rest leads to substantial muscle atrophy and induces whole-body insulin resistance in the absence of skeletal muscle lipid accumulation. Diabetes 65, 2862–2875.
24. Dunstan DW, Howard B, Healy GN & Owen N (2012a). Too much sitting – a health hazard. Diabetes Res Clin Pract 97, 368–376.
25. Dunstan DW, Kingwell BA, Larsen R, Healy GN, Cerin E, Hamilton MT, Shaw JE, Bertovic DA, Zimmet PZ, Salmon J & Owen N (2012b). Breaking up prolonged sitting reduces postprandial glucose and insulin responses. Diabetes Care 35, 976–983.
26. Faerch K & Vaag A (2011). Metabolic inflexibility is a common feature of impaired fasting glycaemia and impaired glucose tolerance. Acta Diabetol 48, 349–353.
27. Flatt JP (1995). Use and storage of carbohydrate and fat. Am J Clin Nutr 61, 952s–959s.
28. Flatt JP (2004). Carbohydrate-fat interactions and obesity examined by a two-compartment computer model. Obes Res 12, 2013–2022.
29. Friedlander AL, Casazza GA, Horning MA, Buddinger TF & Brooks GA (1998). Effects of exercise intensity and training on lipid metabolism in young women. Am J Physiol Endocrinol Metab 275, E853–E863.
30. Galgani JE, Heilbronn LK, Azuma K, Kelley DE, Albu JB, Pi-Sunyer X, Smith SR & Ravussin E (2008a). Metabolic flexibility in response to glucose is not impaired in people with type 2 diabetes after controlling for glucose disposal rate. Diabetes 57, 841–845.
31. Galgani JE, Moro C & Ravussin E (2008b). Metabolic flexibility and insulin resistance. Am J Physiol Endocrinol Metab 295, E1009–E1017.
32. Galgani J & Ravussin E (2008). Energy metabolism, fuel selection and body weight regulation. Int J Obes (Lond) 32 Suppl 7, S109–S119.
33. Gaster M (2007). Metabolic flexibility is conserved in diabetic myotubes. J Lipid Res 48, 207–217.
34. Gerich JE (2002). Is reduced first-phase insulin release the earliest detectable abnormality in individuals destined to develop type 2 diabetes? Diabetes 51 Suppl 1, S117–S121.
35. Hamilton MT, Hamilton DG & Zderic TW (2014). Sedentary behavior as a mediator of type 2 diabetes. Med Sport Sci 60, 11–26.
36. Healy GN, Dunstan DW, Salmon J, Cerin E, Shaw JE, Zimmet PZ & Owen N (2008). Breaks in sedentary time: beneficial associations with metabolic risk. Diabetes Care 31, 661–666.
37. Healy GN, Matthews CE, Dunstan DW, Winkler EA & Owen N (2011). Sedentary time and cardio-metabolic biomarkers in US adults: NHANES 2003–06. Eur Heart J 32, 590–597.
38. Holmstrup M, Fairchild T, Keslacy S, Weinstock R & Kanaley J (2014). Multiple short bouts of exercise over 12-h period reduce glucose excursions more than an energy-matched single bout of exercise. Metabolism 63, 510–519.
39. Kelley DE, Goodpaster B, Wing RR & Simoneau JA (1999). Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol Endocrinol Metab 277, E1130–E1141.
40. Kelley DE & Mandarino LJ (1990). Hyperglycemia normalizes insulin-stimulated skeletal muscle glucose oxidation and storage in noninsulin-dependent diabetes mellitus. J Clin Invest 86, 1999–2007.
41. Kelley DE & Mandarino LJ (2000). Fuel selection in human skeletal muscle in insulin resistance: a reexamination. Diabetes 49, 677–683.
42. Kelley DE, Mokan M & Mandarino LJ (1992). Intracellular defects in glucose metabolism in obese patients with NIDDM. Diabetes 41, 698–706.
43. Kelley DE & Simoneau JA (1994). Impaired free fatty acid utilization by skeletal muscle in non-insulin-dependent diabetes mellitus. J Clin Invest 94, 2349–2356.
44. Larsen RN, Kingwell BA, Robinson C, Hammond L, Cerin E, Shaw JE, Healy GN, Hamilton MT, Owen N & Dunstan DW (2015). Breaking up of prolonged sitting over three days sustains, but does not enhance, lowering of postprandial plasma glucose and insulin in overweight and obese adults. Clin Sci (Lond) 129, 117–127.
45. Lee IM, Shiroma EJ, Lobelo F, Puska P, Blair SN & Katzmarzyk PT (2012). Impact of physical inactivity on the world's major non-communicable diseases. Lancet 380, 219–229.
46. Levine JA, Vander Weg MW, Hill JO & Klesges RC (2006). Non-exercise activity thermogenesis: the crouching tiger hidden dragon of societal weight gain. Arterioscler Thromb Vasc Biol 26, 729–736.
47. Lyden K, Keadle SK, Staudenmayer J, Braun B & Freedson PS (2015). Discrete features of sedentary behavior impact cardiometabolic risk factors. Med Sci Sports Exerc 47, 1079–1086.
48. Malin SK, Haus JM, Solomon TP, Blaszczak A, Kashyap SR & Kirwan JP (2013a). Insulin sensitivity and metabolic flexibility following exercise training among different obese insulin-resistant phenotypes. Am J Physiol Endocrinol Metab 305, E1292–E1298.
49. Malin SK, Solomon TPJ, Blaszczak A, Finnegan S, Filion J & Kirwan JP (2013b). Pancreatic β-cell function increases in a linear dose-response manner following exercise training in adults with prediabetes. Am J Physiol Endocrinol Metab 305, E1248–E1254.
50. Martin GM (1966). Hazards of inactivity. JAMA 196, 909–910.
51. Mikines KJ, Sonne B, Tronier B & Galbo H (1989). Effects of training and detraining on dose-response relationship between glucose and insulin secretion. Am J Physiol Endocrinol Metab 256, E588–E596.
52. Oldridge NB (2008). Economic burden of physical inactivity: healthcare costs associated with cardiovascular disease. Eur J Cardiovasc Prev Rehabil 15, 130–139.
53. Olsen RH, Krogh-Madsen R, Thomsen C, Booth FW & Pedersen BK (2008). Metabolic responses to reduced daily steps in healthy nonexercising men. JAMA 299, 1261–1263.
54. Peddie MC, Bone JL, Rehrer NJ, Skeaff CM, Gray AR & Perry TL (2013). Breaking prolonged sitting reduces postprandial glycemia in healthy, normal-weight adults: a randomized crossover trial. Am J Clin Nutr 98, 358–366.
55. Rynders CA, Weltman JY, Jiang B, Breton M, Patrie J, Barrett EJ & Weltman A (2014). Effects of exercise intensity on postprandial improvement in glucose disposal and insulin sensitivity in prediabetic adults. J Clin Endocrinol Metab 99, 220–228.
56. Schrauwen P, Lichtenbelt WD, Saris WH & Westerterp KR (1998). Fat balance in obese subjects: role of glycogen stores. Am J Physiol Endocrinol Metab 274, E1027–E1033.
57. Schrauwen P, van Marken Lichtenbelt WD, Saris WH & Westerterp KR (1997). Role of glycogen-lowering exercise in the change of fat oxidation in response to a high-fat diet. Am J Physiol Endocrinol Metab 273, E623–E629.
58. Slentz CA, Tanner CJ, Bateman LA, Durheim MT, Huffman KM, Houmard JA & Kraus WE (2009). Effects of exercise training intensity on pancreatic beta-cell function. Diabetes Care 32, 1807–1811.
59. Smith SR, de Jonge L, Zachwieja JJ, Roy H, Nguyen T, Rood J, Windhauser M, Volaufova J & Bray GA (2000). Concurrent physical activity increases fat oxidation during the shift to a high-fat diet. Am J Clin Nutr 72, 131–138.
60. Sparks LM, Pasarica M, Sereda O, deJonge L, Thomas S, Loggins H, Xie H, Miles JM & Smith SR (2009a). Effect of adipose tissue on the sexual dimorphism in metabolic flexibility. Metabolism 58, 1564–1571.
61. Sparks LM, Ukropcova B, Smith J, Pasarica M, Hymel D, Xie H, Bray GA, Miles JM & Smith SR (2009b). Relation of adipose tissue to metabolic flexibility. Diabetes Res Clin Pract 83, 32–43.
62. Stephens BR, Granados K, Zderic TW, Hamilton MT & Braun B (2011). Effects of 1 day of inactivity on insulin action in healthy men and women: interaction with energy intake. Metabolism 60, 941–949.
63. Stubbs RJ, Hughes DA, Johnstone AM, Whybrow S, Horgan GW, King N & Blundell J (2004). Rate and extent of compensatory changes in energy intake and expenditure in response to altered exercise and diet composition in humans. Am J Physiol Regul Integr Comp Physiol 286, R350–R358.
64. Thorp AA, Kingwell BA, Sethi P, Hammond L, Owen N & Dunstan DW (2014). Alternating bouts of sitting and standing attenuate postprandial glucose responses. Med Sci Sports Exerc 46, 2053–2061.
65. Thyfault JP, Rector RS & Noland RC (2006). Metabolic inflexibility in skeletal muscle: a prelude to the cardiometabolic syndrome? J Cardiometab Syndr 1, 184–189.
66. Ukropcova B, Sereda O, de Jonge L, Bogacka I, Nguyen T, Xie H, Bray GA & Smith SR (2007). Family history of diabetes links impaired substrate switching and reduced mitochondrial content in skeletal muscle. Diabetes 56, 720–727.
67. van Dijk JW, Venema M, van Mechelen W, Stehouwer CD, Hartgens F & van Loon LJ (2013). Effect of moderate-intensity exercise versus activities of daily living on 24-hour blood glucose homeostasis in male patients with type 2 diabetes. Diabetes Care 36, 3448–3453.