The Effect of Pistacia Atlantica Extract and Aerobic Training on the Levels of Triiodothyronine, Thyroxine and Lipid Profile in Streptozotocin-Diabetic Rats

Document Type: Original Article

Authors

1 Associate Professor, Department of Animal Science, Faculty of Agriculture, University of Birjand, Birjand, Iran

2 Master of Science, Department of Animal Science, Faculty of Agriculture, University of Birjand, Birjand, Iran

3 Associate Professor, Department of Exercise Physiology, Faculty of Sport Sciences, University of Birjand, Birjand, Iran

4 Master of Science Department of Exercise Physiology, Faculty of Sport Sciences, University of Birjand, Birjand, Iran

Abstract

Background: Diabetes is considered as one of the health problems in all societies. Exercise training and herbal medicines are some approaches to improve diabetes. The present study investigated the effect of a six weeks exercise training program and/or Pistacia atlantica (mastic) extract on thyroid hormones and lipid profile as well as antidiabetic effects in diabetic rats.
Methods: Forty male Wistar rats were randomly divided into five groups: Healthy control (Ctrl), diabetic control (D), Diabetic + exercise (DE), Diabetic + mastic extract (DM) and Diabetic + exercise + mastic extract (DEM). The six-week period exercise program included aerobic training on a treadmill (five sessions per week, 40 minutes per each session, with a speed of 20 m/min and 5% incline). Pistacia atlantica extract was fed 5 days per week (25 mg/kg). Forty eight hours after the last training session, the level of T3, T4, triglyceride, cholesterol and HDL were assessed.
Results:Triglyceride levels in DEM group was significantly lower than diabetic group (p<0.05). The mean level of cholesterol and HDL (high density lipoprotein) was not significantly different among groups. Plasma concentration of T
3
and T
4
in diabetic control was significantly lower than normal control. Applying mastic extract alone or together with exercise markedly enhanced T4 levels in diabetic rats.
Conclusion: Pistacia atlantica extract and exercise training might be good in the improvement of hypothyroidism and hyperlipidemia resulting from diabetes.

Keywords


  1. Chiasson JL, Rabasa-Lhoret R. Prevention of type 2 diabetes: insulin resistance and beta-cell function. Diabetes 2004; 53(suppl 3):S34-8.
  2. Sheetz MJ, King GL. Molecular understanding of hyperglycemia's adverse effects for diabetic complications. JAMA 2002; 288(20):2579-88.
  3. Karamifar H, Amirhakimi GH. Goiter and hypothyroidism in children with insulin dependent diabetes mellitus. Feyz Journal of Kashan University of Medical Sciences 2004; 7(4):95-100. [In Persian].
  4. Centers for Disease Control and Prevention. National diabetes fact sheet, 2011. [cited 2015 Jun 17] Available from: http://www.diabetesincontrol.com/wp-content/uploads/PDF/ndep_diabetes_facts_2011.pdf
  5. Ezike AC, Akah PA, Okoli CO, Udegbunam S, Okwume N, Okeke C, et al. Medicinal plants used in wound care: A study of Prosopis africana (Fabaceae) stem bark. Indian J Pharm Sci 2010; 72(3):334-9.
  6. Grover J, Yadav S, Vats V. Medicinal plants of India with anti-diabetic potential. J Ethnopharmacol 2002; 81(1):81-100.
  7. Lanhers MC, Joyeux M, Soulimani R, Fleurentin J, Sayag M, Mortier F, et al. Hepatoprotective and anti-inflammatory effects of a traditional medicinal plant of Chile, Peumus boldus. Planta Med 1991; 57(2):110-5.
  8. Ahmadabad SR, Ansari Pirsaraei Z, Ghanbari Niaki A, Deldar H, Zare Kookandeh N, Shahandeh F. Effect of 8 weeks treadmill running with or without pistachia atlantica liquid extraction on liver ABCG8 gene expression and cholesterol level in female rat. Iranian Journal of Health and Physical Activity 2012; 3(1):43-9.
  9. Rahimi N, Marandi SM, Kargarfard M. The effect of eight weeks aquatic training on lipid profile of patients who suffer from type II diabetes. Journal of Isfahan Medical School. 2011; 29(148):988-96. [In Persian].
  10. Karizno FM, Saghebjoo M, Foadoddini M, Sarir H. The role of aerobic training and pistacia atlantica extract on the levels of protein carbonyl, heat shock protein 70, and glycogen in the liver tissue of diabetic rats. Journal of Birjand University of Medical Sciences 2014; 21(1):35-47. [In Persian].
  11. Hatamnia AA, Abbaspour N, Darvishzadeh R. Antioxidant activity and phenolic profile of different parts of Bene (pistacia atlantica subsp. kurdica) fruits. Food Chem 2014; 145:306-11.
  12. Singh M, Kaur M, Silakari O. Flavones: An important scaffold for medicinal chemistry. Eur J Med Chem 2014; 84:206-39.
  13. Nijveldt RJ, Van Nood E, Van Hoorn DE, Boelens PG, Van Norren K, Van Leeuwen PA. Flavonoids: a review of probable mechanisms of action and potential applications. Am J Clin Nutr 2001; 74(4):418-25.
  14. Jacob RA. The integrated antioxidant system. Nutrition research 1995; 15(5):755-66.
  15. Christensen KB, Minet A, Svenstrup H, Grevsen K, Zhang H, Schrader E, et al. Identification of plant extracts with potential antidiabetic properties: effect on human peroxisome proliferator-activated receptor (PPAR), adipocyte differentiation and insulin-stimulated glucose uptake. Phytother Res 2009; 23(9):1316-25.
  16. Craig WJ. Health-promoting properties of common herbs. Am J Clin Nutr 1999; 70(3 Suppl):491s-9s.
  17. Tanwar B, Modgil R. Flavonoids: Dietary occurrence and health benefits. Spatula DD 2012; 2(1):59-68.
  18. Parker B, Noakes M, Luscombe N, Clifton P. Effect of a high-protein, high–monounsaturated fat weight loss diet on glycemic control and lipid levels in type 2 diabetes. Diabetes care 2002; 25(3):425-30.
  19. Kashi Z, Akha O, Boroumand M, Bahar A, Mobini M. The correlation between type 2 diabetes mellitus and hypothyroidism. Journal of Mazandaran University of Medical Sciences 2010; 20(79):9-14. [In Persian].
  20. Hage M, Zantout MS, Azar ST. Thyroid disorders and diabetes mellitus. J Thyroid Res 2011; 2011:439463.
  21. Perros P, McCrimmon RJ, Shaw G, Frier BM. Frequency of thyroid dysfunction in diabetic patients: value of annual screening. Diabet Med 1995; 12(7):622-7.
  22. Loucks AB, Callister R. Induction and prevention of low-T3 syndrome in exercising women. Am J Physiol 1993; 264(5 Pt 2):R924-30.
  23. González C, Montoya E, Jolín T. Effect of streptozotocin diabetes on the hypothalamic-pituitary-thyroid axis in the rat. Endocrinology 1980; 107(6):2099-103.
  24. Saeb M, Nazifi S, Beizaee A, Gheisari HR, Jalaee J. Effect of wild pistachio oil on serum leptin concentration and thyroid hormones in the male rat. Iranian Journal of Endocrinology and Metabolism 2008; 9(4):429-37. [In Persian].
  25. Junod A, Lambert AE, Stauffacher W, Renold AE. Diabetogenic action of streptozotocin: relationship of dose to metabolic response. J Clin Invest 1969; 48(11):2129-39.
  26. Zarekar M, Saghebjoo M, Foadodini M, Hedayati M. Combined effect of aerobic training and pistacia athlantica extract on GLUT-4 protein expression and muscle glycogen in diabetic rats. Iranian Journal of Endocrinology and Metabolism 2014; 16(4):245-53. [In Persian].
  27. Winer B. Statistical principles in experimental design, 2nd ed. New York: McGraw-Hill; 1971.
  28. Ceriello A. New insights on oxidative stress and diabetic complications may lead to a "causal" antioxidant therapy. Diabetes care 2003; 26(5):1589-96.
  29. Ihara Y, Toyokuni S, Uchida K, Odaka H, Tanaka T, Ikeda H, et al. Hyperglycemia causes oxidative stress in pancreatic beta-cells of GK rats, a model of type 2 diabetes. Diabetes 1999; 48(4):927-32.
  30. Rolo AP, Palmeira CM. Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress. Toxicol Appl Pharmacol 2006; 212(2):167-78.
  31. Uttara B, Singh AV, Zamboni P, Mahajan RT. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol 2009; 7(1):65-74.
  32. Ishige K, Schubert D, Sagara Y. Flavonoids protect neuronal cells from oxidative stress by three distinct mechanisms. Free Radic Biol Med 2001; 30(4):433-46.
  33. Lobo V, Patil A, Phatak A, Chandra N. Free radicals, antioxidants and functional foods: impact on human health. Pharmacogn Rev 2010; 4(8):118-26.
  34. Mezni F, Shili S, Ben Ali N, Larbi Khouja M, Khaldi A, Maaroufi A. Evaluation of pistacia lentiscus seed oil and phenolic compounds for in vitro antiproliferative effects against BHK21 cells. Pharm Biol 2016; 54(5):747-51.
  35. Abdeldjelil MC, Bensegueni A, Messai A, Agabou A, Benazzouz H. Medicinal use of pistacia lentiscus fixed oil in Constantine province, north-east Algeria. Journal of Natural Product And Plant Resources 2014; 4(1):48-51. [In Persian].
  36. Bok SH, Lee SH, Park YB, Bae KH, Son KH, Jeong TS, et al. Plasma and hepatic cholesterol and hepatic activities of 3-hydroxy-3-methyl-glutaryl-CoA reductase and acyl CoA: cholesterol transferase are lower in rats fed citrus peel extract or a mixture of citrus bioflavonoids. J Nutr 1999; 129(6):1182-5.
  37. Silaste ML, Alfthan G, Aro A, Kesäniemi YA, Horkko S. Tomato juice decreases LDL cholesterol levels and increases LDL resistance to oxidation. Br J Nutr 2007; 98(6):1251-8.
  38. Daoued KB, Chouaibi M, Gaout N, Haj OB, Hamdi S. Chemical composition and antioxidant activities of cold pressed lentisc (Pistacia lentiscus l.) seed oil. La Rivista Italiana Delle Sostanze Grasse 2016; 93(1):31-8.
  39. Farzanegi P, Mousavi M, Ghanbari-Niaki A. Effect of Pistacia atlantica extract on glutathione peroxidase tissue levels and total oxidative capacity of liver and plasma lipid profile of rats. Zahedan journal of research in medical sciences2013; 15(11):59-63.
  40. Kwiterovich PO Jr. The metabolic pathways of high-density lipoprotein, low-density lipoprotein, and triglycerides: a current review. Am J Cardiol 2000; 86(12A):5L-10L.
  41. Maritim A, Sanders RA, Watkins JB 3rd. Diabetes, oxidative stress, and antioxidants: a review. J Biochem Mol Toxicol 2003; 17(1):24-38.
  42. Wang S, Soni KG, Semache M, Casavant S, Fortier M, Pan L, et al. Lipolysis and the integrated physiology of lipid energy metabolism. Mol Genet Metab 2008; 95(3):117-26.
  43. Deykin D, Vaughan M. Release of free fatty acids by adipose tissue from rats treated with triiodothyronine or propylthiouracil. Journal of Lipid Research 1963; 4(2):200-3.
  44. Bilezikian JP, Loeb JN. The influence of hyperthyroidism and hypothyroidism on α and adrenergic receptor systems and adrenergic responsiveness. Endocr Rev 1983; 4(4):378-88.
  45. Blennemann B, Leahy P, Kim TS, Freake HC. Tissue-specific regulation of lipogenic mRNAs by thyroid hormone. Molecular and Cellular Endocrinology 1995; 110(1-2):1-8.
  46. Oppenheimer JH, Schwartz HL, Lane JT, Thompson MP. Functional relationship of thyroid hormone-induced lipogenesis, lipolysis, and thermogenesis in the rat. J Clin Invest 1991; 87(1):125-32.
  47. Park SY, Lee SP. Effectiveness of crowberry on plasma total antioxidant status, lipid profile and homocysteine. J Food Nutr Res 2013; 1(4):37-41.
  48. Mohammadi Karizno F, Saghebjoo M, Foadoddini M, Sarir H. The role of aerobic training and pistacia atlantica extract on the levels of protein carbonyl, heat shock protein 70, and glycogen in the liver tissue of diabetic rats. Journal of Birjand University of Medical Sciences 2014; 21(1):35-47.