Acute effects of concentric and eccentric exercise matched for energy expenditure on glucose metabolism in healthy females: a randomized crossover trial

Marc Philippe, Georg Junker, Hannes Gatterer, Andreas Melmer, Martin Burtscher, Marc Philippe, Georg Junker, Hannes Gatterer, Andreas Melmer, Martin Burtscher

Abstract

Background: Single bouts of muscle damaging eccentric exercise (EE) affect glucose metabolism negatively while single bouts of concentric (CE) and not muscle damaging eccentric exercise have positive acute short-term effects on glucose metabolism. It has been proposed that long-term endurance EE might be more effective in improving glucose metabolism than long-term CE when adjusted for energy expenditure. This would imply that adaptations of glucose metabolism are dependent on the type of exercise. Interleukin-6 (IL-6) released from the exercising muscles may be involved in and could therefore explain acute adaptations on glucose metabolism. The aim of the study was to investigate the effects of a single bout of CE and a single bout of EE inducing no or just mild muscle damage, matched for energy expenditure, on glucose metabolism.

Methods: 7 healthy but sedentary female participants (age 20.7 ± 2.9 years; BMI 22.45 ± 1.66 kg m(-2); VO2peak 39.0 ± 4.5 ml kg(-1) min(-1)) took part in a randomized cross over trial consisting of 1 h uphill (CE) respectively downhill (EE) walking on a treadmill. Venous blood samples were drawn before, directly after and 24 h after exercise. An oral glucose tolerance test (OGTT) was performed before and 24 h after exercise.

Results: CE and EE lead to comparable changes of glucose tolerance (area under the curve of the OGTT) (-16.0 ± 25.81 vs. -6.3 ± 45.26 mg dl(-1) h(-1), p = 1.000) and HOMA insulin resistance (-0.16 ± 1.53 vs. -0.08 ± 0.75, p = 0.753). Compared to baseline, IL-6 concentration increased significantly immediately after EE (1.07 ± 0.67 vs. 1.32 ± 0.60 pg ml(-1), p = 0.028) and tended to increase immediately after CE (0.75 ± 0.29 vs. 1.03 ± 0.21 pg ml(-1), p = 0.058). TNF-α concentration decreased significantly immediately after EE (1.47 ± 0.19 vs. 1.06 ± 0.29 pg ml(-1), p = 0.046) but not after CE (1.27 ± 0.43 vs. 1.24 ± 0.43 pg ml(-1), p = 0.686) compared to baseline.

Conclusions: Acute effects of a single bout of exercise inducing no or just mild muscle damage on glucose tolerance and insulin resistance seem to be primarily energy expenditure dependent whereas acute anti-inflammatory activity induced by a single bout of exercise appears to be rather exercise type dependent.

Trial registration: NCT01890876, clinicaltrials.gov, https://clinicaltrials.gov/.

Keywords: Concentric exercise; Eccentric exercise; Glucose metabolism; Interleukin 6; Tumor necrosis factor alpha.

Figures

Fig. 1
Fig. 1
Immediate changes of interleukin 6 (IL-6) concentration (#significant change within EE; *tendential change within CE); baseline = PRE, immediately after exercise = stat POST
Fig. 2
Fig. 2
Immediate changes of tumor necrosis factor alpha (TNF-α) concentration (# significant change within EE; ‡significant interaction between CE and EE); baseline = PRE, immediately after exercise = stat POST

References

    1. Asp S, Daugaard JR, Kristiansen S, Kiens B, Richter EA. Eccentric exercise decreases maximal insulin action in humans: muscle and systemic effects. J Physiol. 1996;494:891–898. doi: 10.1113/jphysiol.1996.sp021541.
    1. Camillo CA, Burtin C, Hornikx M, Demeyer H, de Bent K, van Remoortel H, Osadnik CR, Janssens W, Troosters T. Physiological responses during downhill walking: a new exercise modality for subjects with chronic obstructive pulmonary disease? Chron Respir Dis. 2015;12:155–164. doi: 10.1177/1479972315575717.
    1. Carey AL, Steinberg GR, Macaulay SL, Thomas WG, Holmes AG, Ramm G, Prelovsek O, Hohnen-Behrens C, Watt MJ, James DE, Kemp BE, Pedersen BK, Febbraio MA. Interleukin-6 increases insulin-stimulated glucose disposal in humans and glucose uptake and fatty acid oxidation in vitro via AMP-activated protein kinase. Diabetes. 2006;55:2688–2697. doi: 10.2337/db05-1404.
    1. del Aguila LF, Krishnan RK, Ulbrecht JS, Farrell PA, Correll PH, Lang CH, Zierath JR, Kirwan JP. Muscle damage impairs insulin stimulation of IRS-1, PI 3-kinase, and Akt-kinase in human skeletal muscle. Am J Physiol Endocrinol Metab. 2000;279:206–212.
    1. Doyle JA, Sherman WM, Strauss RL. Effects of eccentric and concentric exercise on muscle glycogen replenishment. J Appl Physiol. 1993;74:1848–1855.
    1. Drexel H, Saely CH, Langer P, Loruenser G, Marte T, Risch L, Hoefle G, Aczel S. Metabolic and anti-inflammatory benefits of eccentric endurance exercise—a pilot study. Eur J Clin Invest. 2008;38:218–226. doi: 10.1111/j.1365-2362.2008.01937.x.
    1. Febbraio MA, Pedersen BK. Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. FASEB J. 2002;16:1335–1347. doi: 10.1096/fj.01-0876rev.
    1. Green MS, Doyle JA, Ingalls CP, Benardot D, Rupp JC, Corona BT. Adaptation of insulin-resistance indicators to a repeated bout of eccentric exercise in human skeletal muscle. Int J Sport Nutr Exerc Metab. 2010;20:181–190. doi: 10.1123/ijsnem.20.3.181.
    1. Ide K, Higaki Y, Nishizumi M, Kiyonaga A, Shindo M, Tanaka H. Impaired non-insulin mediated glucose uptake after downhill running in rats. Life Sci. 1996;59:1601–1605. doi: 10.1016/0024-3205(96)00491-2.
    1. Johnson AT, Benjamin MB, Silverman N. Oxygen consumption, heat production, and muscular efficiency during uphill and downhill walking. Appl Ergon. 2002;33:485–491. doi: 10.1016/S0003-6870(02)00031-5.
    1. Kirwan JP, del Aguila LF. Insulin signalling, exercise and cellular integrity. Biochem Soc Trans. 2003;31:1281–1285. doi: 10.1042/bst0311281.
    1. Kirwan JP, Hickner RC, Yarasheski KE, Kohrt WM, Wiethop BV, Holloszy JO. Eccentric exercise induces transient insulin resistance in healthy individuals. J Appl Physiol. 1992;72:2197–2202. doi: 10.1063/1.351611.
    1. Le Floch JP, Escuyer P, Baudin E, Baudon D, Perlemuter L. Blood glucose area under the curve. Methodological aspects. Diabetes Care. 1990;13:172–175. doi: 10.2337/diacare.13.2.172.
    1. MacDonald C, Wojtaszewski JFP, Pedersen BK, Kiens B, Richter EA. Interleukin-6 release from human skeletal muscle during exercise: relation to AMPK activity. J Appl Physiol. 2003;95:2273–2277. doi: 10.1152/japplphysiol.00242.2003.
    1. Maeo S, Yamamoto M, Kanehisa H. Muscular adaptations to short-term low-frequency downhill walking training. Int J Sports Med. 2015;36:150–156.
    1. Marcus RL, Lastayo PC, Dibble LE, Hill L, McClain DA. Increased strength and physical performance with eccentric training in women with impaired glucose tolerance: a pilot study. J Womens Health. 2009;18:253–260. doi: 10.1089/jwh.2007.0669.
    1. Pedersen BK. Muscular interleukin-6 and its role as an energy sensor. Med Sci Sports Exerc. 2012;44:392–396. doi: 10.1249/MSS.0b013e31822f94ac.
    1. Pedersen BK, Febbraio MA. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev. 2008;88:1379–1406. doi: 10.1152/physrev.90100.2007.
    1. Petersen AMW, Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol. 2005;98:1154–1162. doi: 10.1152/japplphysiol.00164.2004.
    1. Philippe M, Krüsmann P, Mersa L, Eder E, Gatterer H, Melmer A, Ebenbichler C, Burtscher M. Acute effects of concentric and eccentric exercise on glucose metabolism and interleukin-6 concentration in healthy males. Biol Sport. 2016;33:153–158. doi: 10.5604/20831862.1198634.
    1. Pokora I, Kempa K, Chrapusta SJ, Langfort J. Effects of downhill and uphill exercises of equivalent submaximal intensities on selected blood cytokine levels and blood creatine kinase activity. Biol Sport. 2014;31:173–178. doi: 10.5604/20831862.1111434.
    1. Sherman WM, Lash JM, Simonsen JC, Bloomfield SA. Effects of downhill running on the responses to an oral glucose challenge. Int J Sport Nutr. 1992;2:251–259. doi: 10.1123/ijsn.2.3.251.
    1. Starkie R, Ostrowski SR, Jauffred S, Febbraio M, Pedersen BK. Exercise and IL-6 infusion inhibit endotoxin-induced TNF-alpha production in humans. FASEB J. 2003;17:884–886.
    1. Steensberg A, van Hall G, Osada T, Sacchetti M, Saltin B, Klarlund Pedersen B. Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6. J Physiol. 2000;529:237–242. doi: 10.1111/j.1469-7793.2000.00237.x.
    1. Sylow L, Jensen TE, Kleinert M, Mouatt JR, Maarbjerg SJ, Jeppesen J, Prats C, Chiu TT, Boguslavsky S, Klip A, Schjerling P, Richter EA. Rac1 is a novel regulator of contraction-stimulated glucose uptake in skeletal muscle. Diabetes. 2013;62:1139–1151. doi: 10.2337/db12-0491.
    1. Sylow L, Møller LLV, Kleinert M, Richter EA, Jensen TE. Rac1—a novel regulator of contraction-stimulated glucose uptake in skeletal muscle. Exp Physiol. 2014;99:1574–1580. doi: 10.1113/expphysiol.2014.079194.
    1. Sylow L, Møller LLV, Kleinert M, Richter EA, Jensen TE. Stretch-stimulated glucose transport in skeletal muscle is regulated by Rac1. J Physiol. 2015;593:645–656. doi: 10.1113/jphysiol.2014.284281.
    1. Wojtaszewski JFP, Nielsen JN, Richter EA. Invited review: effect of acute exercise on insulin signaling and action in humans. J Appl Physiol. 2002;93:384–392. doi: 10.1152/japplphysiol.00043.2002.
    1. Zeppetzauer M, Drexel H, Vonbank A, Rein P, Aczel S, Saely CH. Eccentric endurance exercise economically improves metabolic and inflammatory risk factors. Eur J Prev Cardiol. 2013;20:577–584. doi: 10.1177/2047487312444236.

Source: PubMed

Sponsorzy i współpracownicy

Warunki medyczne

Interwencje lekowe

3
Subskrybuj