@2024 Afarand., IRAN
ISSN: 2252-0805 The Horizon of Medical Sciences 2016;22(1):27-33
ISSN: 2252-0805 The Horizon of Medical Sciences 2016;22(1):27-33
Effect of Aerobic Training and Pistacia atlantica Extract Consumption on Plasma Levels of Lipocalin-2 and Insulin Resistance Index in Streptozotocin-Induced Diabetic Rats
ARTICLE INFO
Article Type
Original ResearchAuthors
Hosseini M. (*)Shemshaki A. (1)
Saghebjoo M. (2)
Gharari Arefi R. (2)
(*) Physical Education Department, Physical Education & Sport Sciences Faculty, University of Esfahan, Esfahan, Iran
(1) Physical Education Department, Physical Education & Sport Sciences Faculty, Al-Zahra University, Tehran, Iran
(2) Physical Education Department, Physical Education & Sport Sciences Faculty, University of Birjand, Birjand, Iran
Correspondence
Address: Unit 3, No 24, Razavieh 11, Sajadshahr Street, South Khorasan, Birjand, Iran. Postal Code: 9716946178Phone: +985632416951
Fax: +985632202032
hoseyni_mahshid68@yahoo.com
Article History
Received: February 7, 2015Accepted: August 15, 2015
ePublished: December 15, 2015
BRIEF TEXT
… [1-9] Different phenolic compounds in the skin of Pistacia atlantica can reduce rate of the oxidation processes [10]. … [11] The extract of the herb contains antioxidants such as sterol and phytosterol, tocopherol, and total phenol. Tocopherol and phenol can act as antioxidants [12]. … [13-18]
No study was found that investigate the simultaneous effects of an aerobic exercise course with the consumption of the extract of Pistacia atlantica on plasma levels of Lcn2 and insulin resistance index in diabetic rats.
The aim of this study was to determine the effects of aerobic exercises and consumption of the extract of Pistacia atlantica on plasma levels of lipocalin-2 and insulin resistance index in the streptozotocin-induced diabetic male rats
This is an experimental study.
Male Wistar rats aged 12 weeks and weighing 180-240g bought from Research Center of Birjand University of Medical Sciences were studied.
40 rats were studied. The rats were kept in Animal Home of Birjand University of Medical Sciences at standard conditions (21±2°C and 12-hour darkness/light cycle).
40mg per kg of body weight of streptozotocin solvent were injected for 32 rats of 40 as intra-peritoneal. Blood sugar more than 250mg/dl was assumed as diabetes criterion [19]. … [20-30] The diabetic rats were randomly divided into 4 groups containing “diabetic control”, “diabetes + exercise”, “diabetes + exercise + extract”, “diabetes + extract”. Other 8 rats formed “healthy control” group. Ethanol and water solvents were used to produce extract. After every exercise session, 25mg per kg of body weight of extract (5mg of extract per 200g rat body weight) were daily fed to the rats of extract groups as gavage. The extract having been diluted in physiological serum, there was 0.5cc treated material as gavage for every rat weighing 200g. To reach equal conditions, equal volume of water administrated to other rats as gavage. Weight of each rat was measured and recorded one time per week using a scale (Bonso, 322, with 1g sensitivity; Japan). Exercise program was 6-week aerobic exercises on a treadmill and 5 sessions per week at 9-11 a.m. Three stages of the program were as the following. The first stage was to be familiar with laboratory. In the stage, the rats were walking on a treadmill with 5-10m/min speed and a zero degree slope for 10 minutes and 2-3 sessions. The second stage was with faster exercises in a longer period, reached its final conditions (40min exercises and 20m/min speed on a 5-degree slope) after 4 weeks from the beginning of the exercise. In two last weeks of the program, the rats walked on the treadmill with final intensity and period (40min exercises and 20m/min speed on a 5-degree slope) [31]. The rats of control group were attending on a walking session per week (5 minutes and 10m/min speed on a zero degree slope) to be familiar with the treadmill device. After 48hour from the last session and after 12hour fasting, the rats were anesthetized and blood sampling was done from their heart using syringes. Eliza kit (CUSABIOBIOTECH, Wuhan; China) was used to analyze and determine the plasma value of Lcn2. Eliza kit (Mercodia, Uppsala; Sweden) was used to determine the insulin levels of plasma. Insulin resistance was investigates by plasma concentrations of glucose and insulin and “HOMA-IR = (Fasting Glucose of Plasma (mmol/lit) × Fasting Insulin of Plasma (mmol/lit))/22.5” formula [3]. Data was analyzed using SPSS 19 software. Data normalization was assessed using Kolmogorov-Smirnov test. The mean values were compared in the groups, using One-way ANOVA. Post-hoc LSD test was used to compare in pair.
There was a significant difference only in HOMA-IR indices in five groups. There was no significant difference in lipocalin-2 index in five groups (Table 1). There was significantly higher mean HOMA-IR index in diabetic control group than healthy control group. There were significantly lower mean HOMA-IR indices in “diabetes + exercise” and “diabetes + exercise + extract” groups than “diabetic control” group. There was no significant difference in mean HOMA-IR indices between “diabetic control” and “diabetes + extract” groups, “diabetes + exercise” and “diabetes + exercise + extract” groups, “diabetes + extract” and “diabetes + exercise + extract” groups, and “diabetes + extract” and “diabetes + exercise” groups, respectively.
There were reduction in the plasma glucose level, improvement in the insulin resistance, and no significant change in the plasma levels of lipocalin-2 levels after 6-week aerobic exercises and consumption of the extract of Pistacia atlantica. 8-week aerobic exercises and consumption of the extract of Pistacia atlanitica do not affect plasma glucose [22]. There is an increase in the glucose resistance of the rats fed by Pistacia atlantica [23, 24]. There was a reduction in insulin resistance in “diabetic” and “diabetes + exercise + extract” groups compared to “diabetic control” group. Moderate intensity short-term sport activities lead to a reduction in insulin resistance, as well as a better function of Pancreas β cells [28], which are results consistent with the present results. There was no significant change in the Lcn2 levels after 6-week aerobic exercises with or without the consumption of the extract of Pistacia atlantica. In ten marathon runners, there have been higher Lcn2 levels immediately after sport activities, which have come to the base level after 48hours from the activities [29]. There has been an increase in the Lcn2 levels after one session incremental and exhaustive sport activities in the obese persons [30]. There was no significant difference between Lcn2 concentrations before and after 3-month exercises [5]. There is a significant reduction in Lcn2 level due to 8-week endurance and resistance exercises than control group, as well as a significant reduction in glucose and insulin resistance compared to pretest stage in healthy young men [33]. 8-week aerobic exercises leads to Lcn2 reduction [34]. … [35, 36]
Greater sample size and groups consuming different doses of the extract should be studied with different aerobic exercise intensities at longer exercise periods.
Sample volume loss and no possibility to determine the effects of different doses of the extract and to conduct a longer exercise period were of the limitations for the present study.
Through a reduction in the insulin resistance, aerobic exercises can improve a dysfunction caused by diabetes oxidative effects solely or with the consumption of antioxidant extract of Pistacia atlantica (25mg/kg).
The staff of Laboratory Unit of Birjand University of Medical Sciences and manager of Cellular and Molecular Biology Research Center of Endocrinology Institute of Shahid Beheshti University of Medical Sciences are appreciated.
Non-declared
All ethical principles were observed by the researchers.
There was no financial support.
TABLES and CHARTS
Show attach fileCITIATION LINKS
[1]Zimmet PZ, Magliano DJ, Herman WH, Shaw JE. Diabetes: A 21st century challenge. Lancet Diabetes Endocrinol. 2014;2(1):56-64.
[2]Azizi Z, Mansoorpoor S, Sabzehvarifard A, Asaie S, Ranjbar Omrani Gh. Effect of Estradiol valerate on pancreatic beta cells resistance in diabetic female rats by streptozotocin. Iran South Med J. 2014;17(2):107-19. [Persian]
[3]Haghighat N, Vafa M, Eghtesadi S, Heidari I, Hoseini AF. The effects of Tocotrienolsenriched canola oil on glycemic control and oxidative stress in patients with type 2 diabetes: A double blind randomized clinical trial. Razi J Med Sci. 2013;20(109):52-61. [Persian]
[4]Wang Y, Lam KS, Kraegen EW, Sweeney G, Zhang J, Tso AW, et al. Lipocalin-2 is an inflammatory marker closely associated with obesity, insulin resistance, and hyperglycemia in humans. Clin Chem. 2007;53(1):34-41.
[5]Choi K, Kim T, Yoo H, Lee K, Cho G, Hwang T, et al. Effect of exercise training on A-FABP, lipocalin-2 and RBP4 levels in obese women. Clin Endocrinol. 2009;70(4):569-74.
[6]Scheer F, Chan J, Fargnoli J, Chamberland J, Arampatzi K, Shea S, et al. Day/night variations of high-molecular-weight adiponectin and lipocalin-2 in healthy men studied under fed and fasted conditions. Diabetologia. 2010;53(11):2401-5.
[7]Cowland JB, Sørensen OE, Sehested M, Borregaard N. Neutrophil gelatinase-associated lipocalin is up-regulated in human epithelial cells by IL-1β, but not by TNF-α. J Immunol. 2003;171(12):6630-9.
[8]Bahmani P, Halabian R, Masrouri N, Rouhbakhsh M, Ebrahimi M, Nourani M, et al. Induction of heme oxygenase-1 by lipocalin 2 mediated by NF-KB transcription factor. J Iran Anat Sci. 2009;1(27):33-44. [Persian]
[9]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. J Birjand Univ Med Sci. 2014;21(1):35-47. [Persian]
[10]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 J Res Med Sci. 2013;15(11):59-63. [Persian]
[11]Peksel A, Arisan-Atac I, Yanardag R. Evaluation of antioxidant and antiacetylcholinesterase activities of the extracts of Pistacia atlantica Desf. Leaves. J Food Biochem. 2010;34(3):451-76.
[12]Saber-Tehrani M, Givianrad MH, Aberoomand-Azar P, Waqif-Husain S, Jafari Mohammadi SA. Chemical composition of Iran's Pistacia atlantica cold-pressed oil. J Chem. 2013;(2013).
[13]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.
[14]Rashidlamir A, Alizadeh A, Ebrahimiatri A, Dastani M. The effect of four-week period of aerobic exercise with cinnamon consumption on lipoprotein indicates and blood sugar in diabetic female patients (type 2). J Shahid Sadoughi Univ Med Sci. 2013;20(5):605-14. [Persian]
[15]Colberg SR, Sigal RJ, Fernhall B, Regensteiner JG, Blissmer BJ, Rubin RR, et al. Exercise and type 2 diabetes. Diabetes Care. 2010;33(12):e147-67.
[16]Richter EA, Hargreaves M. Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol Rev. 2013;93(3):993-1017.
[17]Bello AI, Owusu-Boakye E, Adegoke BO, Adjei DN. Effects of aerobic exercise on selected physiological parameters and quality of life in patients with type 2 diabetes mellitus. Int J Gen Med. 2011;4:723-7.
[18]Yousefipoor P, Tadibi V, Behpoor N, Parnow A, Delbari M, Rashidi S. The effect of 8-week aerobic and concurrent (aerobic-resistance) exercise training on serum il-6 levels and insulin resistance in type 2 diabetic patients. J Shahid Sadoughi Univ Med Sci. 2013;21(5):619-31.
[19]Chis IC, Baltaru D, Maier M, Muresan A, Clichici S. Effects of quercetin and chronic (training) exercise on oxidative stress status in animals with Streptozotocin-induced diabetes. Bull UASVM Vet Med. 2013;70(1):31-9.
[20]Laghari AQ, Memon S, Nelofar A, Laghari AH. Extraction, identification and antioxidative properties of the flavonoid-rich fractions from leaves and flowers of Cassia angustifolia. Am J Anal Chem. 2011;2(8):871.
[21]Kim HJ, Park JY, Oh SL, Kim YA, So B, Seong JK, et al. Effect of treadmill exercise on interleukin-15 expression and glucose tolerance in zucker diabetic fatty rats. Diabetes Metab J. 2013;37(5):358-64.
[22]Ghanbari Niaki A, Fathi R, Shahandeh F, Yazdani M, Hajizadeh A. The effect of endurance training and Pistacia atlantica (bene) extraction on resting plasma visfatin and lipids levels in female rats. Daneshvar Med. 2011;18(94):53-62. [Persian]
[23]Benhammou N, Bekkara FA, Panovska TK. Antioxidant and antimicrobial activities of the Pistacia lentiscus and Pistacia atlantica extracts. Afr J Pharm Pharmacol. 2008;2(2):022-8.
[24]Kasabri V, AbuDahab R, Afifi FU, Naffa R, Majdalawi L. Modulation of pancreatic MIN6 insulin secretion and proliferation, and extrapancreatic glucose absorption with Achillea santolina, Eryngium creticum and Pistacia atlantica extracts: in vitro evaluation. J Exp Integr Med. 2012;2(3):245-54.
[25]Zinman B, Ruderman N, Campaigne B, Devlin J, Schneider S. Physical activity/exercise and diabetes mellitus. Diabetes Care. 2003;26(Suppl1):S73-7.
[26]Manetta J, Brun JF, Maimoun L, Callis A, Préfaut C, Mercier J. Effect of training on the GH/IGF-I axis during exercise in middle-aged men: relationship to glucose homeostasis. Am J Physiol Endocrinol Metab. 2002;283(5):E929-36.
[27]Gleeson M, Bishop NC, Stensel DJ, Lindley MR, Mastana SS, Nimmo MA. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol. 2011;11(9):607-15.
[28]Bloem CJ, Chang AM. Short-term exercise improves β-cell function and insulin resistance in older people with impaired glucose tolerance. J Clin Endocrinol Metab. 2008;93(2):387-92.
[29]Spiropoulos A, Goussetis E, Margeli A, Premetis E, Skenderi K, Graphakos S, et al. Effect of inflammation induced by prolonged exercise on circulating erythroid progenitors and markers of erythropoiesis. Clin Chem Lab Med. 2010;48(2):199-203.
[30]Damirchi A, Rahmani-Nia F, Mehrabani J. Lipocalin-2: Response to a progressive treadmill protocol in obese and normal-weight men. Asian J Sports Med. 2011;2(1):44.
[31]Hemdahl AL, Gabrielsen A, Zhu C, Eriksson P, Hedin U, Kastrup J, et al. Expression of neutrophil gelatinase–associated lipocalin in atherosclerosis and myocardial infarction. Arterioscler Thromb Vasc Biol. 2006;26(1):136-42.
[32]Owen HC, Roberts SJ, Ahmed SF, Farquharson C. Dexamethasone-induced expression of the glucocorticoid response gene lipocalin 2 in chondrocytes. Am J Physiol Endocrinol Metab. 2008;294(6):1023-34.
[33]Moghadasi M, Mohammadi Domieh M. Effects of resistance versus endurance training on plasma lipocalin-2 in young men. Asian J Sports Med. 2014 ;5(2):108-14.
[34]Mohammadi A, Khajehlandi A. Hs-CRP and adipokin (Lcn2): Response to exercise training in obese men. Biomed Pharmacol J. 2014;7(1):17-22.
[35]Bahadoran Z, Mirmiran P, Hosseinpanah F, Hedayati M, Hosseinpour-Niazi S, Azizi F. Broccoli sprouts reduce oxidative stress in type 2 diabetes: A randomized double-blind clinical trial. Eur J Clin Nutr. 2011;65(8):972-7.
[36]Mahmudzadeh T, Saghebjoo M, Seghatol Eslami A, Hedayati M. Effect of aerobic training and Pistacia atlantica extract consumption on pancreatic β-cells function in streptozotocin-induced diabetic rats. Iran J Diabetes Metab. 2014;13(3):252-62. [Persian]
[2]Azizi Z, Mansoorpoor S, Sabzehvarifard A, Asaie S, Ranjbar Omrani Gh. Effect of Estradiol valerate on pancreatic beta cells resistance in diabetic female rats by streptozotocin. Iran South Med J. 2014;17(2):107-19. [Persian]
[3]Haghighat N, Vafa M, Eghtesadi S, Heidari I, Hoseini AF. The effects of Tocotrienolsenriched canola oil on glycemic control and oxidative stress in patients with type 2 diabetes: A double blind randomized clinical trial. Razi J Med Sci. 2013;20(109):52-61. [Persian]
[4]Wang Y, Lam KS, Kraegen EW, Sweeney G, Zhang J, Tso AW, et al. Lipocalin-2 is an inflammatory marker closely associated with obesity, insulin resistance, and hyperglycemia in humans. Clin Chem. 2007;53(1):34-41.
[5]Choi K, Kim T, Yoo H, Lee K, Cho G, Hwang T, et al. Effect of exercise training on A-FABP, lipocalin-2 and RBP4 levels in obese women. Clin Endocrinol. 2009;70(4):569-74.
[6]Scheer F, Chan J, Fargnoli J, Chamberland J, Arampatzi K, Shea S, et al. Day/night variations of high-molecular-weight adiponectin and lipocalin-2 in healthy men studied under fed and fasted conditions. Diabetologia. 2010;53(11):2401-5.
[7]Cowland JB, Sørensen OE, Sehested M, Borregaard N. Neutrophil gelatinase-associated lipocalin is up-regulated in human epithelial cells by IL-1β, but not by TNF-α. J Immunol. 2003;171(12):6630-9.
[8]Bahmani P, Halabian R, Masrouri N, Rouhbakhsh M, Ebrahimi M, Nourani M, et al. Induction of heme oxygenase-1 by lipocalin 2 mediated by NF-KB transcription factor. J Iran Anat Sci. 2009;1(27):33-44. [Persian]
[9]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. J Birjand Univ Med Sci. 2014;21(1):35-47. [Persian]
[10]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 J Res Med Sci. 2013;15(11):59-63. [Persian]
[11]Peksel A, Arisan-Atac I, Yanardag R. Evaluation of antioxidant and antiacetylcholinesterase activities of the extracts of Pistacia atlantica Desf. Leaves. J Food Biochem. 2010;34(3):451-76.
[12]Saber-Tehrani M, Givianrad MH, Aberoomand-Azar P, Waqif-Husain S, Jafari Mohammadi SA. Chemical composition of Iran's Pistacia atlantica cold-pressed oil. J Chem. 2013;(2013).
[13]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.
[14]Rashidlamir A, Alizadeh A, Ebrahimiatri A, Dastani M. The effect of four-week period of aerobic exercise with cinnamon consumption on lipoprotein indicates and blood sugar in diabetic female patients (type 2). J Shahid Sadoughi Univ Med Sci. 2013;20(5):605-14. [Persian]
[15]Colberg SR, Sigal RJ, Fernhall B, Regensteiner JG, Blissmer BJ, Rubin RR, et al. Exercise and type 2 diabetes. Diabetes Care. 2010;33(12):e147-67.
[16]Richter EA, Hargreaves M. Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol Rev. 2013;93(3):993-1017.
[17]Bello AI, Owusu-Boakye E, Adegoke BO, Adjei DN. Effects of aerobic exercise on selected physiological parameters and quality of life in patients with type 2 diabetes mellitus. Int J Gen Med. 2011;4:723-7.
[18]Yousefipoor P, Tadibi V, Behpoor N, Parnow A, Delbari M, Rashidi S. The effect of 8-week aerobic and concurrent (aerobic-resistance) exercise training on serum il-6 levels and insulin resistance in type 2 diabetic patients. J Shahid Sadoughi Univ Med Sci. 2013;21(5):619-31.
[19]Chis IC, Baltaru D, Maier M, Muresan A, Clichici S. Effects of quercetin and chronic (training) exercise on oxidative stress status in animals with Streptozotocin-induced diabetes. Bull UASVM Vet Med. 2013;70(1):31-9.
[20]Laghari AQ, Memon S, Nelofar A, Laghari AH. Extraction, identification and antioxidative properties of the flavonoid-rich fractions from leaves and flowers of Cassia angustifolia. Am J Anal Chem. 2011;2(8):871.
[21]Kim HJ, Park JY, Oh SL, Kim YA, So B, Seong JK, et al. Effect of treadmill exercise on interleukin-15 expression and glucose tolerance in zucker diabetic fatty rats. Diabetes Metab J. 2013;37(5):358-64.
[22]Ghanbari Niaki A, Fathi R, Shahandeh F, Yazdani M, Hajizadeh A. The effect of endurance training and Pistacia atlantica (bene) extraction on resting plasma visfatin and lipids levels in female rats. Daneshvar Med. 2011;18(94):53-62. [Persian]
[23]Benhammou N, Bekkara FA, Panovska TK. Antioxidant and antimicrobial activities of the Pistacia lentiscus and Pistacia atlantica extracts. Afr J Pharm Pharmacol. 2008;2(2):022-8.
[24]Kasabri V, AbuDahab R, Afifi FU, Naffa R, Majdalawi L. Modulation of pancreatic MIN6 insulin secretion and proliferation, and extrapancreatic glucose absorption with Achillea santolina, Eryngium creticum and Pistacia atlantica extracts: in vitro evaluation. J Exp Integr Med. 2012;2(3):245-54.
[25]Zinman B, Ruderman N, Campaigne B, Devlin J, Schneider S. Physical activity/exercise and diabetes mellitus. Diabetes Care. 2003;26(Suppl1):S73-7.
[26]Manetta J, Brun JF, Maimoun L, Callis A, Préfaut C, Mercier J. Effect of training on the GH/IGF-I axis during exercise in middle-aged men: relationship to glucose homeostasis. Am J Physiol Endocrinol Metab. 2002;283(5):E929-36.
[27]Gleeson M, Bishop NC, Stensel DJ, Lindley MR, Mastana SS, Nimmo MA. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol. 2011;11(9):607-15.
[28]Bloem CJ, Chang AM. Short-term exercise improves β-cell function and insulin resistance in older people with impaired glucose tolerance. J Clin Endocrinol Metab. 2008;93(2):387-92.
[29]Spiropoulos A, Goussetis E, Margeli A, Premetis E, Skenderi K, Graphakos S, et al. Effect of inflammation induced by prolonged exercise on circulating erythroid progenitors and markers of erythropoiesis. Clin Chem Lab Med. 2010;48(2):199-203.
[30]Damirchi A, Rahmani-Nia F, Mehrabani J. Lipocalin-2: Response to a progressive treadmill protocol in obese and normal-weight men. Asian J Sports Med. 2011;2(1):44.
[31]Hemdahl AL, Gabrielsen A, Zhu C, Eriksson P, Hedin U, Kastrup J, et al. Expression of neutrophil gelatinase–associated lipocalin in atherosclerosis and myocardial infarction. Arterioscler Thromb Vasc Biol. 2006;26(1):136-42.
[32]Owen HC, Roberts SJ, Ahmed SF, Farquharson C. Dexamethasone-induced expression of the glucocorticoid response gene lipocalin 2 in chondrocytes. Am J Physiol Endocrinol Metab. 2008;294(6):1023-34.
[33]Moghadasi M, Mohammadi Domieh M. Effects of resistance versus endurance training on plasma lipocalin-2 in young men. Asian J Sports Med. 2014 ;5(2):108-14.
[34]Mohammadi A, Khajehlandi A. Hs-CRP and adipokin (Lcn2): Response to exercise training in obese men. Biomed Pharmacol J. 2014;7(1):17-22.
[35]Bahadoran Z, Mirmiran P, Hosseinpanah F, Hedayati M, Hosseinpour-Niazi S, Azizi F. Broccoli sprouts reduce oxidative stress in type 2 diabetes: A randomized double-blind clinical trial. Eur J Clin Nutr. 2011;65(8):972-7.
[36]Mahmudzadeh T, Saghebjoo M, Seghatol Eslami A, Hedayati M. Effect of aerobic training and Pistacia atlantica extract consumption on pancreatic β-cells function in streptozotocin-induced diabetic rats. Iran J Diabetes Metab. 2014;13(3):252-62. [Persian]