Skip to main content

Advertisement

Springer Nature Link
Log in

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

  • Original Article
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  3. S.R. Colberg, C.R. Grieco, Exercise in the treatment and prevention of diabetes. Curr. Sports Med. Rep. 8, 169–175 (2009)

    PubMed  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  Google Scholar 

  13. M.T. Wallace, C.J. Levy, R.D. Matthews, Use and abuse of HOMA modeling. Diabetes Care 27, 1487–1495 (2004)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  28. L.T. Mackinnon, L.M. Hubinger, Effects of exercise on lipoprotein(a). Sports Med. 28, 11–24 (1999)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

  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)

    PubMed  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

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

Author information

Authors and Affiliations

  1. Department of Physical Education and Sports Science, Aristotle University of Thessaloniki, Ag Ioannis, 62110, Serres, Greece

    Nikolaos P. E. Kadoglou & Ioannis S. Vrabas

  2. 1st Department of Internal Medicine, “Hippokratio” General Hospital of Thessaloniki, Thessaloníki, Greece

    Nikolaos P. E. Kadoglou, Grigorios Fotiadis, Zoi Athanasiadou & Ioulia Vitta

  3. Department of Cardiology, “Bodosakio” General Hospital of Ptolemaida, Ptolemaida, Greece

    Stylianos Lampropoulos

Authors
  1. Nikolaos P. E. Kadoglou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Grigorios Fotiadis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zoi Athanasiadou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ioulia Vitta
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stylianos Lampropoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ioannis S. Vrabas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nikolaos P. E. Kadoglou.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kadoglou, N.P.E., Fotiadis, G., Athanasiadou, Z. et al. The effects of resistance training on ApoB/ApoA-I ratio, Lp(a) and inflammatory markers in patients with type 2 diabetes. Endocrine 42, 561–569 (2012). https://doi.org/10.1007/s12020-012-9650-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-012-9650-y

Keywords

Search

Navigation