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European Journal of Applied Physiology

, Volume 113, Issue 12, pp 2925–2932 | Cite as

A single bout of downhill running transiently increases HOMA-IR without altering adipokine response in healthy adult women

  • A. Z. JamurtasEmail author
  • A. Garyfallopoulou
  • A. A. Theodorou
  • A. Zalavras
  • V. Paschalis
  • C. K. Deli
  • M. G. Nikolaidis
  • I. G. Fatouros
  • Y. Koutedakis
Original Article

Abstract

Purpose

Eccentric exercise-induced muscle damage may cause marked alterations in insulin sensitivity. However, it is not entirely known whether such alterations are also related to changes in adipokine levels. The aim of this study was to investigate the effects of muscle damage due to downhill running on inflammation, insulin sensitivity and selected adipokines related to insulin regulation (adiponectin, visfatin, resistin).

Methods

Data were collected from 12 healthy adult women. Each subject participated in two trials, 4 weeks apart. The first trial was reserved for resting measurements only (control trial), while the second trial involved a 45-min exercise (−15 % slope, ~60 % of VO2max) intervention (exercise trial). Insulin sensitivity (HOMA), creatine kinase activity (CK), delayed onset muscle soreness (DOMS), tumor necrosis factor α (TNF-α), interleukin 6 (IL-6), glucose, insulin, adiponectin, resistin, and visfatin were assessed pre-exercise and 1, 2, 3, and 4 days post-exercise and during the same time points in the control trial.

Results

Analyses revealed that CK, DOMS, TNF-α, IL-6, insulin and HOMA significantly increased (p < 0.05) throughout recovery (days 1–4). Adiponectin and visfatin remained unchanged, while resistin significantly increased (p < 0.05) only 2 days post-exercise. Visfatin was negatively correlated with HOMA at days 1 and 4 of recovery.

Conclusion

Although muscle damage due to downhill running caused a decline of insulin sensitivity, this response was not associated with the changes in adipokine levels.

Keywords

Exercise Glucose Muscle damage Eccentric Cytokines 

Abbreviations

AdipoR1

Adiponectin receptors 1

AdipoR2

Adiponectin receptors 2

BMI

Body mass index

CK

Creatine kinase

DOMS

Delayed onset of muscle soreness

GLUT-4

Glucose transporter type 4

HOMA

Homeostasis model assessment

IL-6

Interleukin 6

IRS-1

Insulin receptor substrate 1

PI-3

Phosphatidylinositol 3-kinase

PBMCs

Peripheral blood mononuclear cells

TNF-α

Tumor necrosis factor-α

VO2

Oxygen consumption

VO2max

Maximal oxygen consumption

Notes

Conflict of interest

The authors declare that there is no conflict of interest.

References

  1. Anderson P, Mehta N, Wolfe M, Hinkle C, Pruscino L, Comiskey L, Tabita-Martinez J, Sellers KF, Rickels MR, Ahima RS, Reilly M (2007) Innate immunity modulates adipokines in humans. J Clin Endocrinol Metab 92:2272–2279PubMedCrossRefGoogle Scholar
  2. Armstrong R (1984) Mechanisms of exercise induced delayed onset muscle soreness: a brief review. Med Sci Sports Exerc 16:529–538PubMedGoogle Scholar
  3. Asp S, Daugaard J, Richter E (1995) Eccentric exercise decreases glucose transporter GLUT4 protein in human skeletal muscle. J Physiol 482(Pt 3):705–712PubMedGoogle Scholar
  4. Balducci S, Zanuso S, Nicolucci A, Fernando F, Cavallo S, Cardelli P, Fallucca S, Alessi E, Letizia C, Jimenez A, Fallucca F, Pugliese G (2010) Anti-inflammatory effect of exercise training in subjects with type 2 diabetes and the metabolic syndrome is dependent on exercise modalities and independent of weight loss. Nutr Metab Cardiovasc Dis 20:608–617PubMedCrossRefGoogle Scholar
  5. Beaton L, Tarnopolsky M, Phillips S (2002) Contraction-induced muscle damage in humans following calcium channel blocker administration. J Physiol 544(Pt 3):849–859PubMedCrossRefGoogle Scholar
  6. Bokarewa M, Nagaev I, Dahlberg L, Smith U, Tarkowski A (2005) Resistin, an adipokine with potent proinflammatory properties. J Immunol 174(9):5789–5795PubMedGoogle Scholar
  7. Carter A, Dobridge J, Hackney A (2001) Influence of estrogen on markers of muscle tissue damage following eccentric exercise. Fiziol Cheloveka 27(5):133–137PubMedGoogle Scholar
  8. Chen M, Chung F, Chang D, Tsai J, Huang H, Shin S, Lee Y (2006) Elevated plasma level of visfatin/pre B cell colony-enhancing actor in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab 91:295–299PubMedCrossRefGoogle Scholar
  9. Chen T, Nosaka K, Tu J (2007) Changes in running economy following downhill running. J Sports Sci 25(1):55–63PubMedCrossRefGoogle Scholar
  10. Choi K, Kim J-Y, Cho G, Baik S, Park H, Kim S (2007) Effect of exercise training on plasma visfatin and eotaxin levels. Eur J Endocrinol 157:437–442PubMedCrossRefGoogle Scholar
  11. Conde J, Scotece M, Gómez R, López V, Gómez-Reino J, Lago F, Gualillo O (2011) Adipokines: biofactors from white adipose tissue. A complex hub among inflammation, metabolism, and immunity. BioFactors 37(6):413–420PubMedCrossRefGoogle Scholar
  12. Del Aguila L, Krishnan R, Ulbrecht J, Farrell P, Correll P, Lang C, Zierath JR, Kirwan J (2000) Muscle damage impairs insulin stimulation of IRS-1, PI 3-kinase, and Akt-kinase in human skeletal muscle. Am J Physiol Endocrinol Metab 279(1):206–212Google Scholar
  13. Dibble L, Hale T, Marcus R, Gerber J, Lastayo P (2006) The safety and feasibility of high-force eccentric resistance exercise in persons with Parkinson’s disease. Arch Phys Med Rehabil 87(9):1280–1282PubMedCrossRefGoogle Scholar
  14. Fasshauer M, Paschke R (2003) Regulation of adipocytokines and insulin resistance. Diabetologia 46(12):1594–1603PubMedCrossRefGoogle Scholar
  15. Fehrenbach E, Schneider M (2006) Trauma-induced systemic inflammatory response versus exercise-induced immunomodulatory effects. Sports Med 36:373–384PubMedCrossRefGoogle Scholar
  16. Franckhauser S, Elias I, Rotter Sopasakis V, Ferré T, Nagaev I, Andersson CX, Agudo J, Ruberte J, Bosch F, Smith U (2008) Overexpression of Il6 leads to hyperinsulinaemia, liver inflammation and reduced body weight in mice. Diabetologia 51(7):1306–1316PubMedCrossRefGoogle Scholar
  17. Fruebis J, Tsao T, Javorschi S, Ebbets-Reed D, Erickson M, Yen F, Bihain BE, Lodish H (2001) Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc Natl Acad Sci USA 98:2005–2010PubMedCrossRefGoogle Scholar
  18. Halberg N, Schraw T, Wang Z, Kim J-Y, Yi J, Hamilton M, Luby-Phelps K, Scherer P (2009) Systemic fate of the adipocyte-derived factor adiponectin. Diabetes 58:1961–1970PubMedCrossRefGoogle Scholar
  19. Haus J, Solomon T, Marchetti C, O’Leary V, Brooks L, Gonzalez F, Kirwan J (2009) Decreased visfatin after exercise training correlates with improved glucose tolerance. Med Sci Sports Exerc 41:1255–1260PubMedCrossRefGoogle Scholar
  20. Heath G, Gavin J III, Hinderliter J, Hag-Berg J, Bloomfield S, Holloszy J (1983) Effects of exercise and lack of exercise on glucose tolerance and insulin sensitivity. J Appl Physiol 55:512–517PubMedGoogle Scholar
  21. Jamurtas A, Theocharis V, Tofas T, Tsiokanos A, Yfanti C, Paschalis V, Koutedakis Y, Nosaka K (2005) Comparison between leg and arm eccentric exercises of the same relative intensity on indices of muscle damage. Eur J Appl Physiol 95(2–3):179–185PubMedCrossRefGoogle Scholar
  22. Jamurtas A, Theocharis V, Koukoulis G, Stakias N, Fatouros I, Kouretas D, Koutedakis Y (2006) The effects of acute exercise on serum adiponectin and resistin levels and their relation to insulin sensitivity in overweight males. Eur J Appl Physiol 97(1):122–126PubMedCrossRefGoogle Scholar
  23. Jürimäe J, Rämson R, Mäestu J, Purge P, Jürimäe T, Arciero P, von Duvillard S (2009) Plasma visfatin and ghrelin response to prolonged sculling in competitive male rowers. Med Sci Sports Exerc 41(1):137–143PubMedCrossRefGoogle Scholar
  24. Keller P, Moller K, Krabbe K, Pedersen B (2003) Circulating adiponectin levels during human endotoxemia. Clin Exp Immunol 134:107–110PubMedCrossRefGoogle Scholar
  25. Kendall B, Eston R (2002) Exercise-induced muscle damage and the potential protective role of estrogen. Sports Med 32(2):103–123PubMedCrossRefGoogle Scholar
  26. Kern P, Di Gregorio G, Lu T, Rassouli N, Ranganathan G (2003) Adiponectin expression from human adipose tissue: relation to obesity, insulin resistance, and tumor necrosis factor-alpha expression. Diabetes 52:1779–1785PubMedCrossRefGoogle Scholar
  27. Kirwan J, del Aguila L (2003) Insulin signalling, exercise and cellular integrity. Biochem Soc Trans 31(Pt 6):1281–1285PubMedCrossRefGoogle Scholar
  28. Kirwan JP, Hickner RC, Yarasheski KE, Kohrt WM, Wiethop BV, Holloszy J (1992) Eccentric exercise induces transient insulin resistance in healthy individuals. J Appl Physiol 72(6):2197–2202PubMedCrossRefGoogle Scholar
  29. Komi P, Buskirk E (1972) Effect of eccentric and concentric muscle conditioning on tension and electrical activity of human muscle. Ergonomics 15:417–434PubMedCrossRefGoogle Scholar
  30. Lastayo P, Larsen S, Smith S, Dibble L, Marcus R (2010) The feasibility and efficacy of eccentric exercise with older cancer survivors: a preliminary study. J Geriatr Phys Ther 33(3):135–140PubMedGoogle Scholar
  31. Matthews D, Hosker J, Rudenski A, Naylor B, Treacher D, Turner R (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28(7):412–419PubMedCrossRefGoogle Scholar
  32. Mikines K, Sonne B, Tronier B, Galbo H (1989) Effects of acute exercise and detraining on insulin action in trained men. J Appl Physiol 66:704–711PubMedCrossRefGoogle Scholar
  33. Moschen A, Gerner R, Tilg H (2010) Pre-B cell colony enhancing factor/NAMPT/visfatin in inflammation and obesity-related disorders. Curr Pharm Des 16(17):1913–1920PubMedCrossRefGoogle Scholar
  34. Nikolaidis M, Paschalis V, Giakas G, Fatouros I, Sakellariou G, Theodorou A, Koutedakis Y, Jamurtas A (2008) Favorable and prolonged changes in blood lipid profile after muscle-damaging exercise. Med Sci Sports Exerc 40(8):1483–1489PubMedCrossRefGoogle Scholar
  35. Ohmori R, Momiyama Y, Kato R, Taniguchi H, Ogura M, Ayaori M, Nakamura H, Ohsuzu F (2005) Associations between serum resistin levels and insulin resistance, inflammation, and coronary artery disease. J Am Coll Cardiol 46:379–380PubMedCrossRefGoogle Scholar
  36. Ouedraogo R, Gong Y, Berzins B, Wu X, Mahadev K, Hough K, Chan L, Goldstein BJ, Scalia R (2007) Adiponectin deficiency increases leukocyte endothelium interactions via upregulation of endothelial cell adhesion molecules in vivo. J Clin Invest 117:1718–1726PubMedCrossRefGoogle Scholar
  37. Paschalis V, Nikolaidis MG, Giakas G, Theodorou AA, Sakellariou GK, Koutedakis Y, Fatouros IG, Jamurtas AZ (2010) Beneficial changes in energy expenditure and lipid profile after eccentric exercise in overweight and lean women. Scand J Med Sci Sports 20(1):103–111CrossRefGoogle Scholar
  38. Paschalis V, Nikolaidis M, Theodorou A, Panayiotou G, Fatouros I, Koutedakis Y, Jamurtas AZ (2011) A weekly bout of eccentric exercise is sufficient to induce health-promoting effects. Med Sci Sports Exerc 43(1):64–73PubMedCrossRefGoogle Scholar
  39. Peake J, Nosaka K, Suzuki K (2005) Characterization of inflammatory responses to eccentric exercise in humans. Exerc Immunol Rev 11:64–85PubMedGoogle Scholar
  40. Pedersen BK (2011) Muscles and their myokines. J Exp Biol 214(Pt 2):337–346. doi: 10.1242/jeb.048074 PubMedCrossRefGoogle Scholar
  41. Rajala MW, Obici S, Scherer PE, Rossetti L (2003) Adipose-derived resistin and gut-derived resistin-like molecule-beta selectively impair insulin action on glucose production. J Clin Invest 111(2):225–230. doi: 10.1172/JCI16521 PubMedGoogle Scholar
  42. Robinson K, Prins J, Venkatesh B (2011) Clinical review: adiponectin biology and its role in inflammation and critical illness. Crit Care 15(2):221PubMedCrossRefGoogle Scholar
  43. Senn J, Klover P, Nowak I, Mooney R (2002) Interleukin-6 induces cellular insulin resistance in hepatocytes. Diabetes 51:3391–3399PubMedCrossRefGoogle Scholar
  44. Sethi J, Vidal-Puig A (2005) Visfatin: the missing link between intra-abdominal obesity and diabetes? Trends Mol Med 11(8):344–347PubMedCrossRefGoogle Scholar
  45. Steppan CM, Bailey ST, Bhat S, Brown EJ, Banerjee RR, Wright CM, Patel HR, Ahima RS, Lazar MA (2001) The hormone resistin links obesity to diabetes. Nature 409(6818):307–312. doi: 10.1038/35053000 PubMedCrossRefGoogle Scholar
  46. Yang W, Lee W, Funahashi T, Tanaka S, Matsuzawa Y, Chao C, Chen CL, Tai TY, Chuang L (2001) Weight reduction increases plasma levels of an adipose-derived anti-inflammatory protein, adiponectin. J Clin Endocrinol Metab 86:3815–3819PubMedCrossRefGoogle Scholar
  47. Yu J, Javorschi S, Hevener A, Kruszynska Y, Norman R, Sinha M, Olefsky J (2002) The effect of thiazolidinediones on plasma adiponectin levels in normal, obese, and type 2 diabetic subjects. Diabetes 51:2968–2974PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • A. Z. Jamurtas
    • 1
    • 2
    Email author
  • A. Garyfallopoulou
    • 3
  • A. A. Theodorou
    • 1
    • 2
  • A. Zalavras
    • 1
    • 2
  • V. Paschalis
    • 1
    • 2
  • C. K. Deli
    • 1
    • 2
  • M. G. Nikolaidis
    • 4
  • I. G. Fatouros
    • 2
    • 5
  • Y. Koutedakis
    • 1
    • 2
    • 6
  1. 1.Department of Physical Education and Sport ScienceUniversity of ThessalyTrikalaGreece
  2. 2.Institute of Human Performance and RehabilitationCentre for Research and Technology–ThessalyVolosGreece
  3. 3.Department of Biochemistry and BiotechnologyUniversity of ThessalyLarissaGreece
  4. 4.Department of Physical Education and Sport ScienceAristotle University of ThessalonikiSerresGreece
  5. 5.Department of Physical Education and Sport ScienceUniversity of ThraceKomotiniGreece
  6. 6.School of Sports, Performing Arts and LeisureUniversity of WolverhamptonWolverhamptonUK

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