The effect of two methods of resistance training with and without blood flow restriction on coagulation indices and blood glucose levels in type 2 diabetic patients

Document Type : Research Paper


1 PhD student in Physical Education and Sports Science, Department of Biological Sciences in Sport, Faculty of Sport Sciences and Health, Shahid Beheshti University, Tehran, Iran

2 Professor, Department of Biological Sciences in Sport, Faculty of Sport Sciences and Health, Shahid Beheshti University, Tehran, Iran

3 Assistant Professor of Hematology, Department of Laboratory Sciences, School of Allied Medical Sciences, Kashan University of Medical Sciences, Kashan, Iran

4 M.Sc of Hematology laboratory, Department of Laboratory Sciences, School of Allied Medical Sciences, Kashan University of Medical Sciences, Kashan, Iran

5 PhD student in biochemistry and sport metabolic, Department of exercise physiology, Faculty of sport sciences, Mazandaran University, Babolsar, Iran

6 M.Sc in Physical Education, Department of Health and Sports Medicine, Faculty of physical education and sport sciences, Tehran University, Tehran, Iran


Introduction: Imbalance of the homeostasis system can lead to blood clot formation. The aim of this study was to investigate the effect of two resistance training methods with and without blood flow restriction on coagulation parameters and blood glucose levels in diabetic patients.
Methods: 41 patients with type 2 diabetes were randomly divided into three groups of resistance training with and without blood flow restriction and the control group. The subjects of the resistance training group with and without flow restriction performed the training for 8 weeks with intensities of 20, 40, 60, 80% of one maximum repetition and 20 and 30% of one maximum repetition, respectively. During this period, the subjects in the control group led a normal life and did not have a regular exercise program.
Coagulation parameters, hematocrit and blood glucose levels were measured before and 48 hours after the last training session. Analysis of variance with intergroup factor and Bonferroni post hoc test were used to evaluate the effect of intervention on quantitative factors. SPSS22 statistical software was used to analyze the data. Significance level was considered for all statistical analyzes P <0.05.
Results: Prothrombin Time index in both groups of resistance training increased significantly compared to the control group (P ‹0.05); But no significant difference was observed in Partial thromboplastin time and hematocrit index (P ›0.05). Fibrinogen factor also decreased in training groups (P ‹0.05). Blood glucose decreased in the resistance training group without restriction of blood flow compared to the control group (P ‹0.05).
Conclusion: Eight weeks of resistance training can prevent thrombosis and sudden onset of cardiovascular disease in patients with type 2 diabetes by reducing fibrinogen levels and increasing the Prothrombin Time index. This type of exercise also plays an insulin-like role by lowering blood sugar levels.


  1. Ershadi Moqadam H, Barati H, Solimani Z, Mohammadi M. Evaluating the Risk Factors of Type II Diabetes in
    Sabzevar. Paramedical Sciences and Military Health. 2017; 12 (1):24-31. [Persian]
    2. Alzahrani SH, Ajjan R. Coagulation and fibrinolysis in diabetes. Diabetes Vasc. Dis. Res. 2010;7(4):260-73.
    3. Sobczak AI, Stewart AJ. Coagulatory defects in type-1 and type-2 diabetes. International journal of molecular
    sciences. 2019;20(24):6345.
    4. Tanaka KA, Key NS, Levy JH. Blood coagulation: hemostasis and thrombin regulation. Anesth Analg 2009;
    5. Ahmadizad S, El-Sayed MS. The effects of graded resistance exercise on platelet aggregation and activation.
    Med Sci Sports Exerc 2003; 35(6):1026-32.
    6. Paton CM, Brandauer J, Weiss EP, Brown MD, Ivey F, Roth SM, et al. Hemostatic response to postprandial
    lipemia before and after exercise training. J Appl Physiol. 2006;101(1):316-21.
  2. 7. Gram AS, Bladbjerg E-M, Skov J, Ploug T, Sjödin A, Rosenkilde M, et al. Three months of strictly controlled
    daily endurance exercise reduces thrombin generation and fibrinolytic risk markers in younger moderately
    overweight men. Eur J Appl Physiol. 2015; 115(6):1331-8.
    8. Hilberg T, Menzel K, Wehmeier UF. Endurance training modifies exercise-induced activation of blood
    coagulation: RCT. Eur J Appl Physiol. 2013; 113(6):1423-30.
    9. Da Cunha Nascimento D, Neto FR, de Santana FS, da Silva RAS, dos Santos-Neto L, Balsamo S. The
    interactions between hemostasis and resistance training: a review. Int. J. Gen. Med. 2012; 5:249
    10. Kupchak BR, Creighton BC, Aristizabal JC, Dunn-Lewis C, Volk BM, Ballard KD, Comstock BA, Maresh CM,
    Kraemer WJ, Volek JS. Beneficial effects of habitual resistance exercise training on coagulation and fibrinolytic
    responses. Thromb. Res. 2013; 131(6):227-34.
    11. Alzahrani SH, Ajjan RA. Coagulation and fibrinolysis in diabetes. Diab Vasc Dis Res. 2010; 7(4):260-73.
    12. Nikokheslat S. The effects of 12 weeks of resistance training on responses to a single session and resting levels
    of hemorheological and coagulation variables of young men. [Dissertation]. Tehran: Faculty of Physical
    Education and Sport Sciences. University of Tehran. 2009. [Persian]
    13. Smith JE, Garbutt G, Lopes P, Pedoe DT. Effects of prolonged strenuous exercise (marathon running) on
    biochemical and haematological markers used in the investigation of patients in the emergency department. Br
    J Sports Med 2004; 38(3):292-94.
    14. Aronson D, Sheikh-Ahmad M, Avizohar O, Kerner A, Sella R, Bartha P, et al. C-Reactive protein is inversely
    related to physical fitness in middle-aged subjects. Atherosclerosis. 2004; 176(1):173-9.
    15. Awodu OA, Famodu AA. Effects of exercise on hemorheological parameters of young nigerian smokers. Turk
    J Med Sci. 2007; 37(1): 11-16.
    16. Baggio G, Donazzan S, Monti D, Mari D, Martini S, Gabelli C, et al. Lipoprotein(a) and lipoprotein profile in
    healthy centenarians: a reappraisal of vascular risk factors. FASEB J. 1998; 12(6):433-7.
    17. Parsian H, Seidalangi SZ,Ghazalian F, Soheili Sh, Khanali F, Shirvani H. Effects of Strength Training on Creactive protein And Plasma Fibrinogen in unexercised Young Men. Scientific Journal of Ilam University of
    Medical Sciences. 2010; 18(3): 1-9.
    18. Rankinen T, Vaisanen S, Penttila I, Rauramaa R. Acute dynamic exercise increases fibrinolytic activity. Thromb
    Haemost 1995; 73(2): 281–6.
    19. Cerneca F, Crocetti G, Gombacci A, Simeone R, Tamaro G, Mangiarotti MA. Variation in hemostatic parameters
    after near- maximum exercise and specific tests in athletes. J Sports Med Phys Fitness. 1999; 39: 31-6.
    20. Amouzad Mahdirajei H, Mirsaiedii M, Fadaei S, Abadei R. Compare the Effect of 4 Weeks of Resistance and
    Aerobic Training on Blood Coagulation and Fibrinolytic Factors in Inactive Older Men. Medical Journal of
    Mashhad University of Medical Sciences 2013; 56(3): 150-158.
    21. Ahmadizad S, EI-Sayed MS. The acute effects of resistance exercise on the main determinants of blood rheology.
    J. Sports Sci. 2005; 23(3): 243.
    22. Simpson RJ, Florida-James G, Whyte GP, Guy K. The effects of intensive, moderate and downhill treadmill
    running on human blood lymphocytes expressing the adhesion/activation molecules CD54 (ICAM-1), CD18 (_2
    integrin) and CD53. Eur J Appl Physiol. 2006; 97(1): 109-21.
    23. Van den Burg PJ, Hospers JE, Mosterd WL, Bouma BN, Huisveld IA. Aging, physical conditioning, and
    exercise-induced changes in hemostatic factors and reaction products. J Appl Physiol. 2000; 88(5):1558-64.
    24. Smith JE. Effects of sternuous exercise on haemostasis. Br J Sports Med 2003; 37:433-435.
    25. El-Sayed MS, Sale C, Jones PGW, Chester M. Blood hemostasis in exercise and training. Med Sci Sports Exerc
    2000; 32:918-925.
    26. Boutcher SH, Meyer BJ, Craig GA, Astheimer L. Plasma lipid and fibrinogen levels in aerobically trained and
    untrained postmenopausal women. J Sports Med Phys Fitness. 2003; 43(2):231-5.
    27. Kiouptsi K, Gambaryan S, Walter E, Walter U, Jurk K, Reinhardt C. Hypoxia impairs agonist-induced integrin
    αIIbβ3 activation and platelet aggregation Hypoxia impairs agonist-induced integrin αIIbβ3 activation and
    platelet aggregation. Sci. Rep. 2017, 7: 7621, 1-9.
    28. Gorodetsky AA, Kirilyuk IA, Khramtsov VV, Komarov DA. Functional electron paramagnetic resonance
    imaging of ischemic rat heart: Monitoring of tissue oxygenation and pH. Magn Reson Med 2016; 76, 350–8.
    29. Li M, Hu J, Miao Y, Shen H, Tao D, Yang Z, Li Q, Xuan SY, Raza W, Alzubaidi S, Haacke EM. In vivo
    measurement of oxygenation changes after stroke using susceptibility weighted imaging filtered phase data.
    PLoS One 2013; 8(5): 63013.
    30. Li KC, Pelc LR, Dalman RL, Wright GA, Hollett MD, Ch'en I, Song CK, Porath TS. In vivo magnetic resonance
    evaluation of blood oxygen saturation in the superior mesenteric vein as a measure of the degree of acute flow
    reduction in the superior mesenteric artery: findings in a canine model. Acad Radiol 1997; 4(1): 21–5.
  3. 31. Ayers L, Stoewhas AC, Ferry B, Latshang TD, Lo Cascio CM, Sadler R, Stadelmann K, Tesler N, Huber R,
    Achermann P, Bloch KE, Kohler M. Circulating levels of cell-derived microparticles are reduced by mild
    hypobaric hypoxia: data from a randomised controlled trial. Eur J Appl Physiol 2014; 114(5):1067-73.
    32. Adamopoulos S, Parissis J, Kroupis C, Georgiadis M, Karatzas D, Karavolias G, et al. Physical training reduces
    peripheral markers of inflammation in patients with chronic heart failure. Eur Heart J. 2001; 22(9):791-7.
    33. Kamath S, Lip GY. Fibrinogen: biochemistry, epidemiology and determinants. Int. J. Med. 2003; 96(10):711-
    34. Sobhani V, Mohammadi MT, Shirvani H, Amini A. Long-Term Effect of High-Intensity Interval and Concurrent
    Exercise on Blood Coagulation and Fibrinolysis Parameters in Non-Athlete Healthy Young Men. Quarterly of
    the Horizon of Medical Sciences 2016; 22(4):329-336.
    35. Bath P, Algert C, Chapman N, Neal B. Association of mean platelet volume with risk of stroke among 3134
    individuals with history of cerebrovascular disease. Stroke. 2004; 35(3):622-6.
    36. Kovalenko VM, Shunkova EI, Gol'dberg GA, Karagaeva LG, Shlafer ID, Epifantseva NN. The effect of finoptin
    on platelet aggregation, blood coagulability and fibrinolysis in patientswith ischemic heart disease during
    physical exercise. Kardiologiia. 1991; 31(9):42-4.
    37. Watts EJ. Haemostatic changes in long-distance runners and their relevance to the prevention of ischaemic heart
    disease. Blood Coagul Fibrinolysis. 1991; 2(2):221-5.
    38. Mirsaiedi M, Mahdiraji HA, Khameslu MB, Mazidi A, Akhundi A. Comparison the effect of aerobic and
    resistance exercises in Sari elderly sedentary men on coagulation and fibrinolytic factors. Annals of Biological
    Research. 2012; 3(5):2083-6.
    39. Ahmadizad S, El-Sayed MS, Maclaren DP. Responses of platelet activation and function to a single bout of
    resistance exercise andrecovery. Clin Hemorheol Microcirc. 2006; 35(1-2):159-68.
    40. Fathei M, Mir E. The effect of 12 resistance training sessions on some coagulation and fibrinolytic factors in
    non-active men. Journal of Practical Studies of Biosciences in Sport. 2015 22; 3(5):56-66.
    41. Hemati Nafar M, Kordi MR, Chubineh S, Chubineh S. The Effect of Six-weeks High Intensity Interval Training
    (HIIT) on Fibrinolytic Factors (t-PA, PAI-1& t-PA/PAI-1) in Sedentary Young men. Journal of Sport
    Biosciences. 2013; 5(3):77-89.
    42. Ghalavand A, Shakeriyan S, Monazamnezhad A, Delaramnasab M. The Effect of Resistance Training on CardioMetabolic Factors in Males with Type 2 Diabetes. Jundishapur J Chronic Dis Care. 2014; 3(4): 23346.
    43. Schneider SH, Amorosa LF, Khachadurian AK, Ruderman NB. Studies on the mechanism of improved glucose
    control during regular exercise in type 2 (non-insulin-dependent) diabetes. Diabetologia. 1984; 26(5):355–60.
    44. Rogers MA, Yamamoto C, King DS, Hagberg JM, Ehsani AA, Holloszy JO. Improvement in glucose tolerance
    after 1 wk of exercise in patients with mild NIDDM. Diabetes Care. 1988; 11(8):613–8.
    45. Misra A, Alappan NK, Vikram NK, Goel K, Gupta N, Mittal K, et al. Effect of supervised progressive resistanceexercise training protocol on insulin sensitivity, glycemia, lipids, and body composition in Asian Indians with
    type 2 diabetes. Diabetes Care. 2008; 31(7):1282–7.
    46. Bacchi E, Negri C, Zanolin ME, Milanese C, Faccioli N, Trombetta M, et al. Metabolic effects of aerobic training
    and resistance training in type 2 diabetic subjects: a randomized controlled trial (the RAED2 study). Diabetes
    Care. 2012; 35(4):676–82.
    47. Zanuso S, Jimenez A, Pugliese G, Corigliano G, Balducci S. Exercise for the management of type 2 diabetes: a
    review of the evidence. Acta diabetologica. 2010; 47(1):15-22.
    48. Saghebjoo M, Shabanpoor Omali J, Fathi R. Effects of 8 weeks high intensity circuit resistance training on
    plasma chemerin levels and glycemic control in male patients with type 2 diabetes. Olympic. 2013; 21(3):99-
    49. Cartee GD, Young DA, Sleeper MD, Zierath J, Wallberg-Henriksson H, Holloszy J. Prolongedincrease in
    insulin-stimulated glucose transport in muscle after exercise. Americ Phyio Metabol J. 1989;256(4):494–9
    50. Kern M, Wells JA, Stephens JM, Elton CW, Friedman JE, Tapscott EB, et al. Insulin responsiveness in skeletal
    muscle is determined by glucose transporter (Glut4) protein level. Biochem J. 1990; 270(2):397–400.
    51. Rhee EJ. Chemerin: a novel link between inflammation and atherosclerosis? Diabetes Metabol J; 35(3): 216-
    52. Wang Y, Simar D, Fiatarone Singh MA. Adaptations to exercise training within skeletal muscle in adults with
    type 2 diabetes or impaired glucose tolerance: a systematic review. Diabetes Metab Res Rev. 2009; 25(1):13–
  4. 53. Teixeira-Lemos E, Nunes S, Teixeira F, Reis F. Regular physical exercise training assists in preventing type 2
    diabetes development: focus on its antioxidant and anti-inflammatory properties. Cardio Diabetol J. 2011;
    54. Andersson AK, Flodstrom M, Sandler S. Cytokine-induced inhibition of insulin release from mouse pancreatic
    beta-cells deficient in inducible nitric oxide synthase. Biochem Biophys Res Commun. 2001; 281(2):396–403.
    55. Wang C, Guan Y, Yang J. Cytokines in the progression of pancreatic β-Cell dysfunction 2010. Inter endocrinol
    J. 2010.
    56. Stumvoll M, Goldstein BJ, van Haeften TW. Type 2 diabetes: principles of pathogenesis and therapy. The
    Lancet. 2005; 365(9467):1333–46.
    57. Nayak BS, Ramsingh D, Gooding S, Legall G, Bissram S, Mohammed A, et al. Plasma adiponectin levels are
    related to obesity, inflammation, blood lipids and insulin in type 2 diabetic and non-diabetic Trinidadians. Prim
    Care Diabetes. 2010; 4(3):187–92.
    58. Goldberg RB. Cytokine and cytokine-like inflammation markers, endothelial dysfunction, and imbalanced
    coagulation in development of diabetes and its complications. J Clin
    59. Endocrinol Metab. 2009; 94(9):3171–82.
    60. Kelley DE. Skeletal muscle fat oxidation: timing and flexibility are everything. J Clin Invest. 2005; 115(7):1699–
    61. Kirbas S, Tetik S, Aaykora E, Duran B. An examination of the impact of regular exercise participation on blood
    platelet parameters. World J Med Sci 2015; 12(2):79-82
    62. Nemati GR, Rahmani nia F, Mirzaei B. Eccentric contraction effect on blood hematological parameters in
    untrained young men. Research on Educational Sport 2012; 4(15):71-82. [Persian
    63. Kurdi MR, Ahmadizad S, Dabbagh Nikokhaslat S, Gaini AA, Ravasi AA, Ebrahimi H, Movasheghpour AA,
    Bebri SH. The effect of 12 weeks of resistance training on resting levels of hemorheological variables in young
    men. Journal of Research in Sports Science 2010; 27: 105-122.
    64. Kordi N, Khosravi N. The Effect of 8 Weeks of Mult –Joint and Single–Joint Resistance Training on Some
    Coagulation and Blood Factors in Active Young Men. Journal of Neyshabur University of Medical Sciences
    2017; 5(2): 77-88.