, Volume 42, Issue 3, pp 561–569 | Cite as

The effects of resistance training on ApoB/ApoA-I ratio, Lp(a) and inflammatory markers in patients with type 2 diabetes

  • Nikolaos P. E. Kadoglou
  • Grigorios Fotiadis
  • Zoi Athanasiadou
  • Ioulia Vitta
  • Stylianos Lampropoulos
  • Ioannis S. Vrabas
Original Article


The purpose of this study was to investigate the effects of resistance training (RT) on novel cardiovascular risk factors in patients with type 2 diabetes mellitus (T2DM). We enrolled 52 overweight/obese, type 2 diabetic patients, with inadequate glycemic control (HbA1c > 6.5 %), but without overt diabetic vascular complications. Participants were randomly assigned into two equivalent groups (n = 26): (1) Resistance exercise group: subjects underwent a supervised RT program (3-times/week, 60 min/session, 2–3 sets of 8 machine-weight exercises, 60–80 % of one-repetition maximum). (2) Control group (CG): at study entrance, they received a structured exercise counseling to increase daily physical activity. Clinical parameters, cardiorespiratory capacity, glycemic and lipid profile, apolipoprotein A-I (ApoA-I), apolipoprotein B (ApoB), Lipoprotein(a) [Lp(a)], insulin resistance (HOMA-IR), high-sensitivity CRP (hsCRP), fibrinogen were measured before and after 3 months. RT significantly reduced glycemic indexes, insulin resistance and systolic blood pressure, compared to CG (p < 0.05). Moreover, exercise-treated patients conferred a remarkable downregulation in ApoB levels (from 135.92 ± 30.97 mg/dL to 85.9 ± 26.46 mg/dL, p < 0.001) as compared to CG (from 126.33 ± 36.59 mg/dL to 116.23 ± 27.52 mg/dL, p = 0.872) (p < 0.001). Similarly, ApoB/ApoA-I ratio was considerably decreased in REG rather than CG (-0.32 ± 0.09 vs 0.02 ± 0.01, p < 0.001). Notably, ApoA-I, Lp(a), hsCRP, fibrinogen, the rest of lipid parameters, body weight and exercise capacity remained unaltered in both groups (p > 0.05). Among variables, HOMA-IR reduction was found to be an independent predictor of changes in ApoB/ApoA-I ratio (R 2 = 0.406, p = 0.041) in REG. Long-term RT ameliorated glycemic control, insulin sensitivity and ApoB/ApoA-I ratio in individuals with T2DM. Although we did not observe significant benefits in the rest of cardiovascular risk factors, our results indicate a merely beneficial impact of RT.


Type 2 diabetes Resistance training Exercise Insulin resistance Apolipoprotein A-I Apolipoprotein B Lp(a) hsCRP 



Nikolaos P.E. Kadoglou was granted by the Alexander S. Onassis Public Benefit Foundation.


  1. 1.
    J.B. Buse, H.N. Ginsberg, G.L. Bakris, N.G. Clark, F. Costa, R. Eckel, V. Fonseca, H.C. Gerstein, S. Grundy, R.W. Nesto, M.P. Pignone, J. Plutzky, D. Porte, R. Redberg, K.F. Stitzel, N.J. Stone, Primary prevention of cardiovascular diseases in people with diabetes mellitus: a scientific statement from the American Heart Association and the American Diabetes Association. Diabetes Care 30, 162–172 (2007)PubMedCrossRefGoogle Scholar
  2. 2.
    D. Umpierre, P.A. Ribeiro, C.K. Kramer, C.B. Leitão, A.T. Zucatti, M.J. Azevedo, J.L. Gross, J.P. Ribeiro, B.D. Schaan, Physical activity advice only or structured exercise training and association with HbA1c levels in type 2 diabetes: a systematic review and meta-analysis. JAMA 305, 1790–1799 (2011)PubMedCrossRefGoogle Scholar
  3. 3.
    S.R. Colberg, C.R. Grieco, Exercise in the treatment and prevention of diabetes. Curr. Sports Med. Rep. 8, 169–175 (2009)PubMedGoogle Scholar
  4. 4.
    N.P. Kadoglou, F. Iliadis, C.D. Liapis, D. Perrea, N. Angelopoulou, M. Alevizos, Beneficial effects of combined treatment with rosiglitazone and exercise on cardiovascular risk factors in patients with type 2 diabetes. Diabetes Care 30, 2242–2244 (2007)PubMedCrossRefGoogle Scholar
  5. 5.
    N.P. Kadoglou, I.S. Vrabas, N. Sailer, A. Kapelouzou, G. Fotiadis, G. Noussios, P.E. Karayannacos, N. Angelopoulou, Exercise ameliorates serum MMP-9 and TIMP-2 levels in patients with type 2 diabetes. Diabetes Metab. 36, 144–151 (2010)PubMedCrossRefGoogle Scholar
  6. 6.
    H.R. Kwon, K.A. Han, Y.H. Ku, H.J. Ahn, B.K. Koo, H.C. Kim, K.W. Min, The effects of resistance training on muscle and body fat mass and muscle strength in type 2 diabetic women. Korean Diabetes J. 34, 101–110 (2010)PubMedCrossRefGoogle Scholar
  7. 7.
    C. Gavin, R.J. Sigal, M. Cousins, M.L. Menard, M. Atkinson, F. Khandwala, G.P. Kenny, S. Proctor, T.C. Ooi, Diabetes Aerobic and Resistance Exercise (DARE) trial investigators. Resistance exercise but not aerobic exercise lowers remnant-like lipoprotein particle cholesterol in type 2 diabetes: a randomized controlled trial. Atherosclerosis 213, 552–557 (2010)PubMedCrossRefGoogle Scholar
  8. 8.
    D. Hansen, P. Dendale, L.J. van Loon, R. Meeusen, The impact of training modalities on the clinical benefits of exercise intervention in patients with cardiovascular disease risk or type 2 diabetes mellitus. Sports Med. 40, 921–940 (2010)PubMedCrossRefGoogle Scholar
  9. 9.
    A. Chudyk, R.J. Petrella, Effects of exercise on cardiovascular risk factors in type 2 diabetes: a meta-analysis. Diabetes Care 34, 1228–1237 (2011)PubMedCrossRefGoogle Scholar
  10. 10.
    J. Leiviskä, J. Sundvall, G. Alfthan, M. Jauhiainen, V. Salomaa, Apolipoprotein A-I, apolipoprotein B, and apolipoprotein B/apolipoprotein A-I ratio: reference intervals compared with values in different pathophysiological conditions from the FINRISK 2007 study. Clin. Chim. Acta 412, 1146–1150 (2011)PubMedCrossRefGoogle Scholar
  11. 11.
    M.R. Taskinen, P.J. Barter, C. Ehnholm, D.R. Sullivan, K. Mann, J. Simes, J.D. Best, S. Hamwood, A.C. Keech, FIELD study investigators. Ability of traditional lipid ratios and apolipoprotein ratios to predict cardiovascular risk in people with type 2 diabetes. Diabetologia 53, 1846–1855 (2010)PubMedCrossRefGoogle Scholar
  12. 12.
    A.N. Qasim, S.S. Martin, N.N. Mehta, M.L. Wolfe, J. Park, S. Schwartz, M. Schutta, N. Iqbal, M.P. Reilly, Lipoprotein(a) is strongly associated with coronary artery calcification in type-2 diabetic women. Int. J. Cardio. l150, 17–21 (2011)CrossRefGoogle Scholar
  13. 13.
    M.T. Wallace, C.J. Levy, R.D. Matthews, Use and abuse of HOMA modeling. Diabetes Care 27, 1487–1495 (2004)PubMedCrossRefGoogle Scholar
  14. 14.
    W.R. Sukala, R. Page, D.S. Rowlands, J. Krebs, I. Lys, M. Leikis, J. Pearce, B.S. Cheema, South Pacific Islanders resist type 2 diabetes: comparison of aerobic and resistance training. Eur. J. Appl. Physiol. 112, 317–325 (2012)PubMedCrossRefGoogle Scholar
  15. 15.
    D.W. Dunstan, R.M. Daly, N. Owen, D. Jolley, M. De Courten, J. Shaw, P. Zimmet, High-intensity resistance training improves glycemic control in older patients with type 2 diabetes. Diabetes Care 25, 1729–1736 (2002)PubMedCrossRefGoogle Scholar
  16. 16.
    T.S. Church, S.N. Blair, S. Cocreham, N. Johannsen, W. Johnson, K. Kramer, C.R. Mikus, V. Myers, M. Nauta, R.Q. Rodarte, L. Sparks, A. Thompson, C.P. Earnest, Effects of aerobic and resistance training on hemoglobin A1c levels in patients with type 2 diabetes: a randomized controlled trial. JAMA 304, 2253–2262 (2010)PubMedCrossRefGoogle Scholar
  17. 17.
    E. Cauza, U. Hanusch-Enserer, B. Strasser, B. Ludvik, S. Metz-Schimmerl, G. Pacini, O. Wagner, P. Georg, R. Prager, K. Kostner, A. Dunky, P. Haber, The relative benefits of endurance and strength training on the metabolic factors and muscle function of people with type 2 diabetes mellitus. Arch. Phys. Med. Rehabil. 86, 1527–1533 (2005)PubMedCrossRefGoogle Scholar
  18. 18.
    S. Terada, T. Yokozeki, K. Kawanaka, K. Ogawa, M. Higuchi, O. Ezaki, I. Tabata, Effects of high-intensity swimming training on GLUT-4 and glucose transport activity in rat skeletal muscle. J. Appl. Physiol. 90, 2019–2024 (2001)PubMedGoogle Scholar
  19. 19.
    G.A. Kelley, K.S. Kelley, Progressive resistance exercise and resting blood pressure: a meta-analysis of randomized controlled trials. Hypertension 35, 838–843 (2000)PubMedCrossRefGoogle Scholar
  20. 20.
    B. Strasser, U. Siebert, W. Schobersberger, Resistance training in the treatment of the metabolic syndrome: a systematic review and meta-analysis of the effect of resistance training on metabolic clustering in patients with abnormal glucose metabolism. Sports Med. 40, 397–415 (2010)PubMedCrossRefGoogle Scholar
  21. 21.
    C.M. Ballantyne, T.C. Andrews, J.A. Hsia, J.H. Kramer, C. Shear, ACCESS Study Group. Correlation of non-high-density lipoprotein cholesterol with apolipoprotein B: effect of 5 hydroxymethylglutaryl coenzyme a reductase inhibitors on non-high-density lipoprotein cholesterol levels. Am. J. Cardiol. 88, 265–269 (2001)PubMedCrossRefGoogle Scholar
  22. 22.
    W.C. Cromwell, T.A. Barringer, Low-density lipoprotein and apolipoprotein B: clinical use in patients with coronary heart disease. Curr. Cardiol. Rep. 11, 468–475 (2009)PubMedCrossRefGoogle Scholar
  23. 23.
    G. Walldius, I. Jungner, I. Holme, A. Aastveit, W. Kolar, E. Steiner, High apolipoprotein B, low apolipoprotein A-I, and improvement in the prediction of fatal myocardial infarction (AMORIS study): a prospective study. Lancet 358, 2026–2033 (2001)PubMedCrossRefGoogle Scholar
  24. 24.
    N.P. Kadoglou, F. Iliadis, N. Sailer, Z. Athanasiadou, I. Vitta, A. Kapelouzou, P.E. Karayannacos, C.D. Liapis, M. Alevizos, N. Angelopoulou, I.S. Vrabas, Exercise training ameliorates the effects of rosiglitazone on traditional and novel cardiovascular risk factors in patients with type 2 diabetes mellitus. Metabolism 59, 599–607 (2010)PubMedCrossRefGoogle Scholar
  25. 25.
    M. Stolinski, S. Alam, N.C. Jackson, F. Shojaee-Moradie, C. Pentecost, W. Jefferson, E.R. Christ, R.H. Jones, A.M. Umpleby, Effect of 6-month supervised exercise on low-density lipoprotein apolipoprotein B kinetics in patients with type 2 diabetes mellitus. Metabolism 57, 1608–1614 (2008)PubMedCrossRefGoogle Scholar
  26. 26.
    M. Rigla, J.L. Sánchez-Quesada, J. Ordóñez-Llanos, T. Prat, A. Caixàs, O. Jorba, J.R. Serra, A. de Leiva, A. Pérez, Effect of physical exercise on lipoprotein(a) and low-density lipoprotein modifications in type 1 and type 2 diabetic patients. Metabolism 49, 640–647 (2000)PubMedCrossRefGoogle Scholar
  27. 27.
    S.Y. Jae, K.S. Heffernan, M.K. Lee, B. Fernhall, W.H. Park, Relation of cardiorespiratory fitness to inflammatory markers, fibrinolytic factors, and lipoprotein(a) in patients with type 2 diabetes mellitus. Am. J. Cardiol. 102, 700–703 (2008)PubMedCrossRefGoogle Scholar
  28. 28.
    L.T. Mackinnon, L.M. Hubinger, Effects of exercise on lipoprotein(a). Sports Med. 28, 11–24 (1999)PubMedCrossRefGoogle Scholar
  29. 29.
    L.K. Stewart, M.G. Flynn, W.W. Campbell, B.A. Craig, J.P. Robinson, K.L. Timmerman, B.K. McFarlin, P.M. Coen, E. Talbert, The influence of exercise training on inflammatory cytokines and C-reactive protein. Med. Sci. Sports Exerc. 39, 1714–1719 (2007)PubMedCrossRefGoogle Scholar
  30. 30.
    N.P. Kadoglou, F. Iliadis, N. Angelopoulou, D. Perrea, G. Ampatzidis, C.D. Liapis, M. Alevizos, The anti-inflammatory effects of exercise training in patients with type 2 diabetes mellitus. Eur. J. Cardiovasc. Prev. Rehabil. 14, 837–843 (2007)PubMedCrossRefGoogle Scholar
  31. 31.
    A. Chudyk, R.J. Petrella, Effects of exercise on cardiovascular risk factors in type 2 diabetes: a meta-analysis. Diabetes Care 34, 1228–1237 (2011)PubMedCrossRefGoogle Scholar
  32. 32.
    D.L. Swift, N.M. Johannsen, C.P. Earnest, S.N. Blair, T.S. Church: Effect of exercise training modality on C-reactive protein in type-2 diabetes. Med. Sci. Sports Exerc. (2011) (Epub ahead of print)Google Scholar
  33. 33.
    H.E. Ploeger, T. Takken, M.H. de Greef, B.W. Timmons, The effects of acute and chronic exercise on inflammatory markers in children and adults with a chronic inflammatory disease: a systematic review. Exerc. Immunol. Rev. 15, 6–41 (2009)PubMedGoogle Scholar
  34. 34.
    S. Balducci, S. Zanuso, A. Nicolucci, F. Fernando, S. Cavallo, P. Cardelli, S. Fallucca, E. Alessi, C. Letizia, A. Jimenez, F. Fallucca, G. Pugliese, 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 (2010)PubMedCrossRefGoogle Scholar
  35. 35.
    C.L. Clarson, F.H. Mahmud, J.E. Baker, H.E. Clark, W.M. McKay, V.D. Schauteet, D.J. Hill, Metformin in combination with structured lifestyle intervention improved body mass index in obese adolescents, but did not improve insulin resistance. Endocrine 36, 141–146 (2009)PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Nikolaos P. E. Kadoglou
    • 1
    • 2
  • Grigorios Fotiadis
    • 2
  • Zoi Athanasiadou
    • 2
  • Ioulia Vitta
    • 2
  • Stylianos Lampropoulos
    • 3
  • Ioannis S. Vrabas
    • 1
  1. 1.Department of Physical Education and Sports ScienceAristotle University of ThessalonikiSerresGreece
  2. 2.1st Department of Internal Medicine“Hippokratio” General Hospital of ThessalonikiThessaloníkiGreece
  3. 3.Department of Cardiology“Bodosakio” General Hospital of PtolemaidaPtolemaidaGreece

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