Swimming, but not vitamin E, ameliorates prothrombotic state and hypofibrinolysis in a rat model of nonalcoholic fatty liver disease
-
Hussein F. Sakr
,
Amr M. Abbas
Abstract
Background:
Nonalcoholic fatty liver disease (NAFLD) is associated with a systemic procoagulant hypofibrinolysis state that is considered as a risk factor for microangiopathy and peripheral vascular diseases. Swimming exercise ameliorates the metabolic dysfunction in type 2 diabetes. Vitamin E is a natural antioxidant that reduces the risk of endothelial dysfunction in metabolic syndrome. The aim of the present study is to investigate the effect of combined swimming exercise with vitamin E on coagulation as well as blood fibrinolysis markers in rats with NAFLD.
Methods:
Eighty male rats were divided into control, control+vitamin E, control+exercise, high-fat diet (HFD), HFD+vitamin E, HFD+exercise, and HFD+vitamin E+exercise groups. Glucose, insulin, homeostatic model assessment for insulin resistance (HOMA-IR), triglycerides, cholesterol, low-density lipoprotein (LDL) and high-density lipoprotein (HDL), alanine transaminase (ALT) and aspartate transaminase (AST), intercellular adhesion molecule (ICAM-1), vascular cell adhesion molecule (VCAM-1), endothelin-1, von Willebrand factor (vWF), fibrinogen, plasminogen activator inhibitor (PAI-1), fibrin degradation products (FDP), platelet count and aggregation, bleeding and clotting times, activated partial thromboplastin time (aPTT), and prothrombin time (PT) were determined.
Results:
HFD increased lipid profile, insulin, glucose, HOMA-IR, liver enzymes, adhesion molecules, endothelin-1, vWF, platelet aggregation, fibrinogen, FDP, and PAI-1, and decreased clotting and bleeding times and HDL. Although exercise reduced lipid profile, glucose, insulin, HOMA-IR, vWF, platelet aggregation, fibrinogen, FDP, and PAI-1 and increased PT, aPTT, bleeding and clotting times, and HDL, vitamin E had no effect.
Conclusions:
Exercise, but not vitamin E, ameliorated the HFD-induced prothrombotic state and enhanced fibrinolytic activity.
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: None declared.
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.
References
1. Willebrords J, Pereira IV, Maes M, Crespo Yanguas S, Colle I, Van Den Bossche B, et al. Strategies, models and biomarkers in experimental non-alcoholic fatty liver disease research. Prog Lipid Res 2015;59:106–25.10.1016/j.plipres.2015.05.002Suche in Google Scholar PubMed PubMed Central
2. Targher G, Arcaro G. Non-alcoholic fatty liver disease and increased risk of cardiovascular disease. Atherosclerosis 2007;191:235–40.10.1016/j.atherosclerosis.2006.08.021Suche in Google Scholar PubMed
3. Kotronen A, Yki-Jarvinen H. Fatty liver: a novel component of the metabolic syndrome. Arterioscler Thromb Vasc Biol 2008;28:27–38.10.1161/ATVBAHA.107.147538Suche in Google Scholar PubMed
4. Milic S, Stimac D. Nonalcoholic fatty liver disease/steatohepatitis: epidemiology, pathogenesis, clinical presentation and treatment. Dig Dis 2012;30:158–62.10.1159/000336669Suche in Google Scholar PubMed
5. Targher G, Chonchol M, Miele L, Zoppini G, Pichiri I, Muggeo M. Nonalcoholic fatty liver disease as a contributor to hypercoagulation and thrombophilia in the metabolic syndrome. Semin Thromb Hemost 2009;35:277–87.10.1055/s-0029-1222606Suche in Google Scholar PubMed
6. Cho J, Kim S, Lee S, Kang H. Effect of training intensity on nonalcoholic fatty liver disease. Med Sci Sports Exerc 2015;47:1624–34.10.1249/MSS.0000000000000595Suche in Google Scholar PubMed
7. Zelber-Sagi S, Nitzan-Kaluski D, Goldsmith R, Webb M, Zvibel I, Goldiner I, et al. Role of leisure-time physical activity in nonalcoholic fatty liver disease: a population-based study. Hepatology 2008;48:1791–8.10.1002/hep.22525Suche in Google Scholar PubMed
8. Ordonez R, Carbajo-Pescador S, Mauriz JL, Gonzalez-Gallego J. Understanding nutritional interventions and physical exercise in non-alcoholic fatty liver disease. Curr Mol Med 2015;15:3–26.10.2174/1566524015666150114110551Suche in Google Scholar PubMed
9. Johnson NA, Sachinwalla T, Walton DW, Smith K, Armstrong A, Thompson MW, et al. Aerobic exercise training reduces hepatic and visceral lipids in obese individuals without weight loss. Hepatology 2009;50:1105–12.10.1002/hep.23129Suche in Google Scholar PubMed
10. Traber MG, Stevens JF. Vitamins C and E: beneficial effects from a mechanistic perspective. Free Radic Biol Med 2011;51:1000–13.10.1016/j.freeradbiomed.2011.05.017Suche in Google Scholar PubMed PubMed Central
11. Di Bella L, Di Bella G. Solution of retinoids in vitamin E in the Di Bella Method biological multitherapy. Neuro Endocrinol Lett 2015;36:661–76.Suche in Google Scholar PubMed
12. Nowak G, Bakajsova D, Hayes C, Hauer-Jensen M, Compadre CM. Gamma-Tocotrienol protects against mitochondrial dysfunction and renal cell death. J Pharmacol Exp Ther 2012;340:330–8.10.1124/jpet.111.186882Suche in Google Scholar PubMed PubMed Central
13. Ekhlasi G, Kolahdouz Mohammadi R, Agah S, Zarrati M, Hosseini AF, Arabshahi SS, et al. Do symbiotic and vitamin E supplementation have favorite effects in nonalcoholic fatty liver disease? A randomized, double-blind, placebo-controlled trial. J Res Med Sci 2016;21:1735–995.10.4103/1735-1995.193178Suche in Google Scholar
14. Abbas AM, Sakr HF. Simvastatin and vitamin E effects on cardiac and hepatic oxidative stress in rats fed on high fat diet. J Physiol Biochem 2013;69:737–50.10.1007/s13105-013-0250-ySuche in Google Scholar PubMed
15. Nascimento AF, Sugizaki MM, Leopoldo AS, Lima-Leopoldo AP, Nogueira CR, Novelli EL, et al. Misclassification probability as obese or lean in hypercaloric and normocaloric diet. Biol Res 2008;41:253–9.10.4067/S0716-97602008000300002Suche in Google Scholar PubMed
16. Sakr HF. Effect of sitagliptin on the working memory and reference memory in type 2 diabetic Sprague–Dawley rats: possible role of adiponectin receptors 1. J Physiol Pharmacol 2013;64:613–23.Suche in Google Scholar PubMed
17. Lillie LE, Temple NJ, Florence LZ. Reference values for young normal Sprague–Dawley rats: weight gain, hematology and clinical chemistry. Hum Exp Toxicol 1996;15:612–6.10.1177/096032719601500802Suche in Google Scholar PubMed
18. Sakr HF, Al-Hashem FH, El-Naby WM, Alkhateeb MA, Zaki MS, Refaey HM, et al. Preventive roles of swimming exercise and pioglitazone treatment on hepatic dysfunction in a rat model of metabolic syndrome. Can J Physiol Pharmacol 2014;92:162–70.10.1139/cjpp-2013-0043Suche in Google Scholar PubMed
19. El-Gendy AA, Abbas AM. Effect of omega-3 fatty acids on haemostatic functions in urocortin-treated obese rats. J Physiol Biochem 2014;70:809–20.10.1007/s13105-014-0350-3Suche in Google Scholar PubMed
20. Cacho J, Sevillano J, de Castro J, Herrera E, Ramos MP. Validation of simple indexes to assess insulin sensitivity during pregnancy in Wistar and Sprague–Dawley rats. Am J Physiol Endocrinol Metab 2008;295:16.10.1152/ajpendo.90207.2008Suche in Google Scholar PubMed
21. Kaji T, Yamamoto C, Sakamoto M, Koizumi F. Endothelin modulation of tissue plasminogen activator release from human vascular endothelial cells in culture. Blood Coagul Fibrinolysis 1992;3:5–10.10.1097/00001721-199202000-00002Suche in Google Scholar PubMed
22. Abbas AM, Sakr HF. Effect of magnesium sulfate and thyroxine on inflammatory markers in a rat model of hypothyroidism. Can J Physiol Pharmacol 2016;94:426–32.10.1139/cjpp-2015-0247Suche in Google Scholar PubMed
23. Koopman J, Haverkate F, Koppert P, Nieuwenhuizen W, Brommer EJ, Van der Werf WG. New enzyme immunoassay of fibrin-fibrinogen degradation products in plasma using a monoclonal antibody. J Lab Clin Med 1987;109:75–84.Suche in Google Scholar PubMed
24. Mustard JF, Hegardt B, Rowsell HC, Macmillan RL. Effect of adenosine nucleotides on platelet aggregation and clotting time. J Lab Clin Med 1964;64:548–59.Suche in Google Scholar PubMed
25. Bi S, Scott KA, Hyun J, Ladenheim EE, Moran TH. Running wheel activity prevents hyperphagia and obesity in Otsuka Long-Evans Tokushima Fatty rats: role of hypothalamic signaling. Endocrinology 2005;146:1676–85.10.1210/en.2004-1441Suche in Google Scholar PubMed
26. Ebal E, Cavalie H, Michaux O, Lac G. Effect of a moderate exercise on the regulatory hormones of food intake in rats. Appetite 2007;49:521–4.10.1016/j.appet.2007.03.007Suche in Google Scholar PubMed
27. Howe SM, Hand TM, Manore MM. Exercise-trained men and women: role of exercise and diet on appetite and energy intake. Nutrients 2014;6:4935–60.10.3390/nu6114935Suche in Google Scholar PubMed PubMed Central
28. Sakr HF. Modulation of metabolic and cardiac dysfunctions by swimming in overweight rats on a high cholesterol and fructose diet: possible role of adiponectin. J Physiol Pharmacol 2013;64:231–40.Suche in Google Scholar PubMed
29. Pettersson J, Hindorf U, Persson P, Bengtsson T, Malmqvist U, Werkstrom V, et al. Muscular exercise can cause highly pathological liver function tests in healthy men. Br J Clin Pharmacol 2008;65:253–9.10.1111/j.1365-2125.2007.03001.xSuche in Google Scholar PubMed PubMed Central
30. Aragno M, Tomasinelli CE, Vercellinatto I, Catalano MG, Collino M, Fantozzi R, et al. SREBP-1c in nonalcoholic fatty liver disease induced by Western-type high-fat diet plus fructose in rats. Free Radic Biol Med 2009;47:1067–74.10.1016/j.freeradbiomed.2009.07.016Suche in Google Scholar PubMed
31. Zorad S, Jezova D, Szabova L, Macho L, Tybitanclova K. Low number of insulin receptors but high receptor protein content in adipose tissue of rats with monosodium glutamate-induced obesity. Gen Physiol Biophys 2003;22:557–60.10.1135/css200306125Suche in Google Scholar PubMed
32. Schenk S, Saberi M, Olefsky JM. Insulin sensitivity: modulation by nutrients and inflammation. J Clin Invest 2008;118:2992–3002.10.1172/JCI34260Suche in Google Scholar PubMed PubMed Central
33. Petibois C, Cassaigne A, Gin H, Deleris G. Lipid profile disorders induced by long-term cessation of physical activity in previously highly endurance-trained subjects. J Clin Endocrinol Metab 2004;89:3377–84.10.1210/jc.2003-031311Suche in Google Scholar PubMed
34. Villanova N, Moscatiello S, Ramilli S, Bugianesi E, Magalotti D, Vanni E, et al. Endothelial dysfunction and cardiovascular risk profile in nonalcoholic fatty liver disease. Hepatology 2005;42:473–80.10.1002/hep.20781Suche in Google Scholar PubMed
35. Pittas AG, Joseph NA, Greenberg AS. Adipocytokines and insulin resistance. J Clin Endocrinol Metab 2004;89:447–52.10.1210/jc.2003-031005Suche in Google Scholar PubMed
36. Muniyappa R, Sowers JR. Role of insulin resistance in endothelial dysfunction. Rev Endocr Metab Disord 2013;14:5–12.10.1007/s11154-012-9229-1Suche in Google Scholar PubMed PubMed Central
37. Romano M, Guagnano MT, Pacini G, Vigneri S, Falco A, Marinopiccoli M, et al. Association of inflammation markers with impaired insulin sensitivity and coagulative activation in obese healthy women. J Clin Endocrinol Metab 2003;88:5321–6.10.1210/jc.2003-030508Suche in Google Scholar PubMed
38. Walther C, Gielen S, Hambrecht R. The effect of exercise training on endothelial function in cardiovascular disease in humans. Exerc Sport Sci Rev 2004;32:129–34.10.1097/00003677-200410000-00002Suche in Google Scholar PubMed
39. Isozaki Y, Yoshida N, Kuroda M, Takagi T, Handa O, Kokura S, et al. Effect of a novel water-soluble vitamin E derivative as a cure for TNBS-induced colitis in rats. Int J Mol Med 2006;17:497–502.10.3892/ijmm.17.3.497Suche in Google Scholar PubMed
40. Badimon L, Hernandez Vera R, Vilahur G. Atherothrombotic risk in obesity. Hamostaseologie 2013;33:259–68.10.5482/HAMO-13-07-0034Suche in Google Scholar PubMed
41. Schafer K, Konstantinides S. Adipokines and thrombosis. Clin Exp Pharmacol Physiol 2011;38:864–71.10.1111/j.1440-1681.2011.05589.xSuche in Google Scholar PubMed
42. Alessi MC, Juhan-Vague I. PAI-1 and the metabolic syndrome: links, causes, and consequences. Arterioscler Thromb Vasc Biol 2006;26:2200–7.10.1161/01.ATV.0000242905.41404.68Suche in Google Scholar PubMed
43. Appel SJ, Harrell JS, Davenport ML. Central obesity, the metabolic syndrome, and plasminogen activator inhibitor-1 in young adults. J Am Acad Nurse Pract 2005;17:535–41.10.1111/j.1745-7599.2005.00083.xSuche in Google Scholar PubMed
44. Alessi MC, Bastelica D, Mavri A, Morange P, Berthet B, Grino M, et al. Plasma PAI-1 levels are more strongly related to liver steatosis than to adipose tissue accumulation. Arterioscler Thromb Vasc Biol 2003;23:1262–8.10.1161/01.ATV.0000077401.36885.BBSuche in Google Scholar PubMed
45. Skurk T, Hauner H. Obesity and impaired fibrinolysis: role of adipose production of plasminogen activator inhibitor-1. Int J Obes Relat Metab Disord 2004;28:1357–64.10.1038/sj.ijo.0802778Suche in Google Scholar PubMed
46. Wang JS. Exercise prescription and thrombogenesis. J Biomed Sci 2006;13:753–61.10.1007/s11373-006-9105-7Suche in Google Scholar PubMed
47. Wisloff U, Stoylen A, Loennechen JP, Bruvold M, Rognmo O, Haram PM, et al. Superior cardiovascular effect of aerobic interval training versus moderate continuous training in heart failure patients: a randomized study. Circulation 2007;115:3086–94.10.1161/CIRCULATIONAHA.106.675041Suche in Google Scholar PubMed
48. Ruslan N-H, Hassan R. A comparative study on platelet activation markers between continuous and intermittent exercise training programs in healthy males. J Hematol 2014;3:72–5.10.14740/jh163wSuche in Google Scholar
49. Womack CJ, Rasmussen JM, Vickers DG, Paton CM, Osmond PJ, Davis GL. Changes in fibrinolysis following exercise above and below lactate threshold. Thromb Res 2006;118:263–8.10.1016/j.thromres.2005.06.016Suche in Google Scholar PubMed
©2018 Walter de Gruyter GmbH, Berlin/Boston
Artikel in diesem Heft
- Frontmatter
- Behavior and Neuroprotection
- Seizure vulnerability and anxiety responses following chronic co-administration and acute withdrawal of caffeine and ethanol in a rat model
- Cardiovascular Function
- Indexes of the erythropoietin level in the blood plasma of chronic heart failure patients with anemia
- Oxidative Stress
- Ameliorative effect of gallic acid on doxorubicin-induced cardiac dysfunction in rats
- Sildenafil, a phosphodiesterase-5 inhibitor, offers protection against carbon tetrachloride-induced hepatotoxicity in rat
- Metabolism
- Antidiabetic potential of polyphenolic-rich fraction of Tamarindus indica seed coat in alloxan-induced diabetic rats
- Effect of L-carnitine on diabetes-induced changes of skeletal muscles in rats
- Inflammation
- Swimming, but not vitamin E, ameliorates prothrombotic state and hypofibrinolysis in a rat model of nonalcoholic fatty liver disease
- Infection
- In vitro ovicidal activity of poly lactic acid curcumin-nisin co-entrapped nanoparticle against Fasciola spp. eggs and its reproductive toxicity
- Phytotherapy
- Assessment of the antioxidant, thrombolytic, analgesic, anti-inflammatory, antidepressant and anxiolytic activities of leaf extracts and fractions of Tetracera sarmentosa (L.) Vahl
- Anti-invasive and antiproliferative effects of Pleurotus ostreatus extract on acute leukemia cell lines
- Letter to the Editor
- Is antiarrhythmic drug effectiveness stable? Extrapolating ICD in different space weather conditions
- Acknowledgment
Artikel in diesem Heft
- Frontmatter
- Behavior and Neuroprotection
- Seizure vulnerability and anxiety responses following chronic co-administration and acute withdrawal of caffeine and ethanol in a rat model
- Cardiovascular Function
- Indexes of the erythropoietin level in the blood plasma of chronic heart failure patients with anemia
- Oxidative Stress
- Ameliorative effect of gallic acid on doxorubicin-induced cardiac dysfunction in rats
- Sildenafil, a phosphodiesterase-5 inhibitor, offers protection against carbon tetrachloride-induced hepatotoxicity in rat
- Metabolism
- Antidiabetic potential of polyphenolic-rich fraction of Tamarindus indica seed coat in alloxan-induced diabetic rats
- Effect of L-carnitine on diabetes-induced changes of skeletal muscles in rats
- Inflammation
- Swimming, but not vitamin E, ameliorates prothrombotic state and hypofibrinolysis in a rat model of nonalcoholic fatty liver disease
- Infection
- In vitro ovicidal activity of poly lactic acid curcumin-nisin co-entrapped nanoparticle against Fasciola spp. eggs and its reproductive toxicity
- Phytotherapy
- Assessment of the antioxidant, thrombolytic, analgesic, anti-inflammatory, antidepressant and anxiolytic activities of leaf extracts and fractions of Tetracera sarmentosa (L.) Vahl
- Anti-invasive and antiproliferative effects of Pleurotus ostreatus extract on acute leukemia cell lines
- Letter to the Editor
- Is antiarrhythmic drug effectiveness stable? Extrapolating ICD in different space weather conditions
- Acknowledgment
