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Effects of exercise on inflammation markers in type 2 diabetic subjects

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Abstract

Endothelial dysfunction and plasma markers of inflammation are significantly increased in type 2 diabetics. Several proinflammatory cytokines, acute-phase proteins, and cell adhesion molecules, such as C-reactive protein (CRP), interleukines (IL), and tumor necrosis factor alpha (TNF-α), seem to play a role in the low-grade systemic inflammation observed in these subjects. Lifestyle changes are necessary to prevent atherosclerosis and cardiovascular events. Physical exercise is known to reduce markers of inflammation by decreasing adipocytokine production and cytokine release from skeletal muscles, endothelial cells, and immune system and also improving antioxidant status. In type 2 diabetics, aerobic and resistance training have different effects on cytokine levels, and the differences in the modalities of exercise (type, duration, and intensity) and especially in the examined population could produce different results. Recent research showed that combined exercise has greater anti-inflammatory effects than aerobic or resistance exercise alone causing a deepest decrease in CRP, IL-6, IL-1β, TNF-α, leptin, and resistin and a higher increase in anti-inflammatory cytokines such as IL-4, IL-10, and adiponectin.

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References

  1. Prestes J, Shiguemoto G, Botero JP, Frollini A, Dias R, Leite R, Pereira G, Magosso R, Baldissera V, Cavaglieri C, Perez S (2009) Effects of resistance training on resistin, leptin, cytokines, and muscle force in elderly post-menopausal women. J Sports Sci 27:1607–1615

    Article  PubMed  Google Scholar 

  2. Garcia C, Feve B, Ferré P, Halimi S, Baizri H, Bordier L, Guiu G, Dupuy O, Bauduceau B, Mayaudon H (2010) Diabetes and inflammation: fundamental aspects and clinical implications. Diabetes Metab 36:327–338

    Article  PubMed  CAS  Google Scholar 

  3. Ray A, Huisman MV, Tamsa JT (2009) The role of inflammation on atherosclerosis, intermediate and clinical cardiovascular endpoints in type 2 diabetes mellitus. Eur J Intern Med 20:253–260

    Article  PubMed  CAS  Google Scholar 

  4. Thomsen SB, Rathcke CN, Zerahn B, Vestergaard H (2010) Increased levels of the calcification marker matrix Gla protein and the inflammatory markers YKL-40 and CRP in patients with type 2 diabetes and ischemic heart disease. Cardiovasc Diab 9:86

    Article  CAS  Google Scholar 

  5. Kajitani N, Shikata K, Nakamura A, Nakatou T, Hiramatsu M, Makino H (2010) Microinflammation is a common risk factor for progression of nephropathy and atherosclerosis in Japanese type 2 diabetes mellitus. Diab Res Clin Pract 88:171–176

    Article  CAS  Google Scholar 

  6. 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 20:608–617

    Article  PubMed  CAS  Google Scholar 

  7. Pearson TA, Mensah GA, Alexabder RW, Anderson JL, Cannon RO 3rd, Criqui M et al (2003) AHA/CDC scientific statement. Markers of inflammation and cardiovascular disease. Application to clinical and public health practice. A statement for healthcare professionals from the Centers for Disease Control and prevention and the American Heart Association. Circulation 107:499–511

    Article  PubMed  Google Scholar 

  8. Swellam M, Sayed Mahmoud M, Abdel-Fatah Ali A (2009) Clinical implications of adiponectin and inflammatory biomarkers in type 2 diabetes mellitus. Dis Markers 27:269–278

    PubMed  CAS  Google Scholar 

  9. Sallam N, Khazaei M, Laher I (2010) Effect of moderate-intensity exercise on plasma C-reactive protein and aortic endothelial function in type 2 diabetic mice. Mediators Inflamm. Epub 2010 Aug 2

  10. Rytter E, Vessby B, Asgard R, Johansson C, Sjoidin A, Abramson-Zetterberg L, Moller L, Basu S (2009) Glycaemic status in relation to oxidative stress and inflammation in well controlled type 2 diabetes subjects. Br J Nutr 101:1423–1426

    Article  PubMed  CAS  Google Scholar 

  11. Hansen D, Dendale P, Beelen M, Jonkers RAM, Mullens A, Corluy L, Meeusen R, Van Loon LJC (2010) Plasma adipokine and inflammatory marker concentrations are altered in obese, as opposed to non-obese, type 2 diabetes patients. Eur J Appl Physiol 109:397–404

    Article  PubMed  CAS  Google Scholar 

  12. Sam S, Haffner S, Davidson MH, D’Agostino RB, Feinstein S, Kondos G, Perez A, Mazzone T (2009) Relation of abdominal fat depots to systemic markers of inflammation in type 2 diabetes. Diabetes Care 32:932–937

    Article  PubMed  CAS  Google Scholar 

  13. Nayak S, Soon SQ, Kunjal R, Ramadoo R, Baptiste O, Persad J, Temull V, Diptee L, Balgobin S (2009) Relationship between adiponectin, inflammatory markers and obesity in type 2 diabetic and non diabetic Trinidadians. Arch Physiol Biochem 115:28–33

    Article  PubMed  CAS  Google Scholar 

  14. Mahajan A, Tabassum R, Chavali S, Dwivedi OP, Bharadwaj M, Tandon N, Bharadwaj D (2009) High-sensitivity C-reactive protein levels and type 2 diabetes in urban North Indians. J Clin Endocrinol Metab 94:2123–2127

    Article  PubMed  CAS  Google Scholar 

  15. Aronson D, Sheikh-Ahmad M, Avizohar O, Kerner A, Sella R, Bartha P, Markiewicz W, Levy I, Brook GJ (2004) C-reactive protein is inversely related to physical fitness in middle-aged subjects. Atherosclerosis 176:173–179

    Article  PubMed  CAS  Google Scholar 

  16. Aronson D, Sella R, Sheikh-Ahmad M, Kerner A, Avizohar O, Rispler S, Bartha P, Markiewicz W, Levy I, Brook GJ (2004) The association between cardiorespiratory fitness and C-reactive protein in subjects with the metabolic syndrome. J Am Coll Cardiol 44:2003–2007

    Article  PubMed  CAS  Google Scholar 

  17. Goldhammer E, Tanchillevitch A, Maor I, Beniamini Y, Rosenschein U, Sagiv M (2005) Exercise training modulates cytokines activity in coronaryhearth disease patients. Int J Cardiol 100:93–99

    Article  PubMed  Google Scholar 

  18. American Diabetes Association (2011) Standards for medical care in diabetes. Diabetes Care 34(S1):S11–S61

    Article  Google Scholar 

  19. Zanuso S, Jimenez A, Pugliese G, Corigliano G, Balducci S (2010) Exercise for the management of type 2 diabetes: a review of evidence. Acta Diabetol 47:15–22

    Article  PubMed  Google Scholar 

  20. Ribeiro F, Alves AJ, Duarte JA, Oliverira J (2010) Is exercise training an effective therapy targeting endothelial dysfunction and vascular wall inflammation? Int J Cardiol 141:214–221

    Article  PubMed  Google Scholar 

  21. Calle MC, Fernandez ML (2010) Effects of resistance training on the inflammatory response. Nutr Res Pract 4:259–269

    Article  PubMed  CAS  Google Scholar 

  22. Petersen AM, Pedersen BK (2006) The role of IL-6 in mediating the anti-inflammatory effects of exercise. J Physiol Pharmacol 57(S10):43–51

    PubMed  Google Scholar 

  23. Drenth JP, Van Uum SH, Van Deuren M, Pesman GJ, Van der Ven-Jongekrijg J, Van der Meer JW (2005) Endurance run increases circulating IL-6 and IL-1ra but downregulates ex vivo TNF-alpha and IL-1 beta production. J Appl Physiol 79:1497–1503

    Google Scholar 

  24. Stewart LK, Flynn MG, Campbell WW, Craig BA, Robinson JP, Timmermann KL, McFarlin BK, Coen PM, Talbert E (2007) The influence of exercise training on inflammatory cytokines and C-reactive protein. Med Sci Sports Exerc 39:1714–1719

    Article  PubMed  CAS  Google Scholar 

  25. Perrier S, Darakhshan F, Hajduch E (2006) IL-1 receptor antagonist in metabolic diseases: Dr Jekyll or Mr Hyde? FEBS Lett 580:6289–6294

    Article  PubMed  CAS  Google Scholar 

  26. Pedersen BK, Febbraio MA (2007) Point: interleukin-6 does have a beneficial role in insulin sensitivity and glucose homeostasis. J Appl Physiol 102:804–806

    Google Scholar 

  27. Prokopchuk O, Liu Y, Wang L, Wirth K, Schimdtbleicher D, Steinacker JM (2007) Skeletal muscle IL-4, IL-4Ralpha, IL13 and IL-13Ralpha1 expression and response to strength training. Exerc Immunol Rev 13:67–75

    PubMed  Google Scholar 

  28. Gordon PL, Vannier E, Hamada K, Layne J, Hurley BF, Roubenoff R, Castaneda-Sceppa C (2006) Resistance training alters cytokine gene expression in skeletal muscle of adults with type 2 diabetes. Int J Immunopatol Pharmacol 19:739–749

    CAS  Google Scholar 

  29. Tantiwong P, Shanmugasundaram K, Monroy A, Ghosh S, Li M, DeFronzo RA, Cersosimo E, Sriwijitkamol A, Mohan S, Musi N (2010) NF-κB activity in muscle from obese and type 2 diabetic subjects under basal and exercise-stimulated conditions. Am J Physiol Endocrinol Metab 299(5):E794–E801. Epub 2010 Aug 24

    Google Scholar 

  30. Santos MJ, Fonseca JE (2009) Metabolic syndrome, inflammation and atherosclerosis–the role of adipokines in health and in systemic inflammatory rheumatic disease. Acta Reumatol Port 34:590–598

    PubMed  Google Scholar 

  31. Wang Z, Nakayama T (2010) Inflammation, a link between obesity and cardiovascular disease. Mediators Inflamm 535918. Epub 2010 Aug 5

  32. Lim S, Choi SH, Jeong IK, Kim JH, Moon MK, Park KS, Lee HK, Kim YB, Jang HK (2008) Insulin-sensitizing effects of exercise on adiponectin and retinol-binding protein-4 concentrations in young and middle-aged women. J Clin Endocrinol Metab 93:2263–2268

    Article  PubMed  CAS  Google Scholar 

  33. Ku YH, Han KA, Ahn H, Kwon H, Koo BK, Kim HC, Min KW (2010) Resistance exercise did not alter intramuscular adipose tissue but reduced retinol-binding protein-4 concentration in individuals with type 2 diabetes mellitus. J Int Med Res 38:782–791

    PubMed  CAS  Google Scholar 

  34. Ahmadizad S, Haghighi AH, Hamedinia MR (2007) Effects of resistance versus endurance training on serum adiponectin and insulin resistance index. Eur J Endocrinol 157:625–631

    Article  PubMed  CAS  Google Scholar 

  35. Ibanez J, Izquierdo M, Martinez-Labari C, Ortega F, Grijalba A, Forga L, Idoate F, Garcia-Unciti M, Fernandez-Real JM, Gorostiaga EM (2010) Resistance training improves cardiovascular risk factors in obese women despite a significant decrease in serum adiponectin levels. Obesity 18:535–541

    Article  PubMed  Google Scholar 

  36. Bloem CJ, Chang AM (2008) Short-term exercise improves cell function and insulin resistance in older people with impaired glucose tolerance. J Clin Endocrinol Metab 93:387–392

    Article  PubMed  CAS  Google Scholar 

  37. Praet SFE, Jonkers RAM, Schep G, Stehouwer CDA, Kuipers H, Keizer HA, Van Loon LJ (2008) Long-standing, insulin-treated type 2 diabetes patients with complications respond well to short-term resistance and interval exercise training. Eur J Endocrinol 158:163–172

    Article  PubMed  CAS  Google Scholar 

  38. Praet SFE, Van Loon LJ (2009) Exercise therapy in type 2 diabetes. Acta Diabetol 46:263–278

    Article  PubMed  Google Scholar 

  39. Brooks N, Layne JE, Gordon PL, Roubenoff R, Nelson ME, Castaneda-Sceppa C (2007) Strength training improves muscle quality and insulin sensitivity in Hispanic older adults with type 2 diabetes. Int J Med Sci 4:19–27

    CAS  Google Scholar 

  40. Simpson KA, Singh MA (2008) Effects of exercise on adiponectin: a systematic review. Obesity 16:241–256

    Article  PubMed  CAS  Google Scholar 

  41. Andersson J, Jansson JH, Hellsten G, Nilsson TK, Hallmans G, Boman K (2010) Effects of heavy endurance physical exercise on inflammatory markers in non-athletes. Atherosclerosis 209:601–605

    Article  PubMed  CAS  Google Scholar 

  42. Nicklas BJ, Ambrosius W, Messier SP, Miller GD, Penninx BWJH, Loeser RF, Palla S, Bleecker E, Pahor M (2004) Diet-induced weight loss, exercise, and chronic inflammation in older, obese adults: a randomized controlled clinical trial. Am J Clin Nutr 79:544–551

    PubMed  CAS  Google Scholar 

  43. You T, Nicklas BJ (2006) Chroonic inflammation: role of adipose tissue and modulation by weight loss. Curr Diabetes Rev 2:29–37

    Article  PubMed  Google Scholar 

  44. Sixt S, Beer S, Bluher M, Korff N, Peschel T, Sonnabend M, Teupser D, Thiery J, Adams V, Schuler G, Niebauer J (2010) Long- but not short-term multifactorial intervention with focus on exercise training improves coronary endothelial dysfunction in diabetes mellitus type 2 and coronary artery disease. Eur Heart J 31:112–119

    Article  PubMed  CAS  Google Scholar 

  45. Kadoglou NP, Iliadis F, Angelopoulou N, Perrea D, Ampatzidis G, Liapis CD, Alevizos M (2007) The anti-inflammatory effects of exercise training in patients with type 2 diabetes mellitus. Eur J Cardiovasc Prev Rehabil 14:837–843

    Google Scholar 

  46. Di Penta JM, Green-Johnson JM, Murphy RJL (2007) Type 2 diabetes mellitus, resistance training, and innate immunity: is there a common link? Appl Physiol Nutr Metab 32:1025–1035

    Article  Google Scholar 

  47. Li ZZ, Liu JB, Jiao L, Chen L (2009) Intensive therapy for diabetes through influence on innate immune system. Med Hypotheses 72:675–676

    Article  PubMed  CAS  Google Scholar 

  48. Troseid M, Lappegard KT, Claudi T, Damas JK, Morkrid L, Brendberg R, Mollness TE (2004) Exercise reduces plasma levels of the chemokines MCP-1 and IL-8 in subjects with the metabolic syndrome. Eur Hearth J 25:349–355

    Article  CAS  Google Scholar 

  49. Troseid M, Lappegard KT, Mollness TE, Arnesen H, Seljeflot I (2009) The effect of exercise on serum levels of IL-18 and components of the metabolic syndrome. Metab Syndr Relat Disord 7:579–584

    Article  PubMed  CAS  Google Scholar 

  50. Oberbach A, Tonjes A, Kloting N, Fasshauer M, Kratzsch J, Busse MW, Paschke R, Stomwoll M, Bluher M (2006) Effect of a 4 week physical training program on plasma concentrations of inflammatory markers in patients with abnormal glucose tolerance. Eur J Endocrinol 154:577–585

    Article  PubMed  CAS  Google Scholar 

  51. Herder C, Peltonen M, Koenig W, Suftels K, Lindstrom J, Martin S, Ilanne-Parikka P, Eriksson JG, Aunola S, Keinanen-Kiukaanniemi S, Valle TT, Uusitopa M, Kolb H, Tuomilehto J (2009) Anti-inflammatory effect of lifestyle changes in the Finnish Diabetes Prevention Study. Diabetologia 52:433–442

    Article  PubMed  CAS  Google Scholar 

  52. Zoppini G, Targher G, Zamboni C, Venturi C, Cacciatori V, Moghetti P, Muggeo M (2006) Effects of moderate-intensity exercise training on plasma biomarkers of inflammation and endothelial dysfunction in older patients with type 2 diabetes. Nutr Metab Cardiovasc Dis 16:543–549

    Article  PubMed  CAS  Google Scholar 

  53. De Salles BF, Simao R, Fleck SJ, Dias I, Kraemer-Aguiar LG, Bouskela E (2010) Effects of resistance training on cytokines. Int J Sports Med 31:441–450

    Article  PubMed  Google Scholar 

  54. Flack KD, Davy KP, Hulver MW, Winett RA, Frisard MI, Davy BM (2010) Aging, resistance training and diabetes prevention. J Aging Res 2011:127315

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Authors and Affiliations

  1. Dipartimento di Medicina Interna, Malattie Cardiovascolari e Nefrourologiche, Università degli Studi di Palermo, Via del Vespro, 129, 90127, Palermo, Italy

    E. Hopps, B. Canino & G. Caimi

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  1. E. Hopps
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  2. B. Canino
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  3. G. Caimi
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Correspondence to E. Hopps.

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Hopps, E., Canino, B. & Caimi, G. Effects of exercise on inflammation markers in type 2 diabetic subjects. Acta Diabetol 48, 183–189 (2011). https://doi.org/10.1007/s00592-011-0278-9

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