@2024 Afarand., IRAN
ISSN: 2252-0805 The Horizon of Medical Sciences 2017;23(4):257-263
ISSN: 2252-0805 The Horizon of Medical Sciences 2017;23(4):257-263
Simultaneous Effect of High-Intensity Interval Training (HIIT) and Consumption of Flaxseed on Serum Levels of TNF-α and IL1β in Rats
ARTICLE INFO
Article Type
Original ResearchAuthors
Khademi Y. (*)Azarbayjani M.A. (1)
Hosseini S.A. (2)
(*) Physical Education Department, Physical Education Faculty, Central Tehran Branch, Islamic Azad University, Tehran, Iran
(1) Sport Physiology Department, Physical Education Faculty, Central Tehran Branch, Islamic Azad University, Tehran, Iran
(2) Sport Physiology Department, Human Science Faculty, Marvdasht Branch, Islamic Azad University, Marvdasht, Iran
Correspondence
Address: Physical Education Department, Physical Education Faculty, Central Tehran Branch, Islamic Azad University, Iran Zamin Street, Tehran, IranPhone: +98 (71) 43112201
Fax: +98 (71) 43311172
youneskhademi3@gmail.com
Article History
Received: November 9, 2016Accepted: March 13, 2017
ePublished: September 28, 2017
BRIEF TEXT
Interleukin-1 beta (IL-1 β) precipitating cytokines and tumor necrosis factor alpha (TNF-α) which increase and stimulate vascular endothelial activity, have been introduced as new inflammatory markers and have high accuracy and sensitivity in predicting cardiovascular diseases. They play an important role in the pathogenesis of atherosclerosis [1-3].
… [4-12]. In a study, it was found that 30 minutes of daily running on a treadmill for one to three weeks was accompanied by significant decrease in the sICAM values (soluble intercellular adhesion molcecule-1) and pro-inflammatory cytokines [13, 14]. In addition, another study found that 12 weeks of aerobic training (3 sessions per week) in rats caused a significant decrease in sICAM-1 and IL1β and TNF-α pro-inflammatory cytokines [15]. … [16-28]. A study also found that the use of flax seed oil would reduce the oxidative stress and reduce the risk of inflammation in dialysis patients [29]. In another study, it was shown that flaxen oil had an effect on inflammatory factor of C-reactive agent in obese people and reduced this inflammatory factor [30].
Regarding the simultaneous effect of exercise and flax seed oil supplementation, only one study was conducted in 2012 and it was found that the simultaneous effect of sport training and supplementation of flaxen oil resulted in a significant decrease in IL1β and TNF-α in rats with ischemic disease [31]. Regarding the physical exercises, also, studies have shown that severity, duration and type of activity are important factors influencing inflammation. Therefore, the present study aimed to investigate the simultaneous effect of intense periodic exercises and the use of flax seed oil supplementation with different doses on TNF-α and IL1β levels in rats.
This study is experimental.
Wistar rats weighing 324.96±38.19 gr and the age of 18 weeks were studied. The animals were kept at a temperature of 22±2 ° C, humidity of 45-50%, and a 12-hour dark-light cycle, and diet for mice was provided for them (Dairy Animal Feed Behparvar Co. Karaj, Iran). Before conducting the research, rats carried the period of adaptability to the laboratory environment.
30 rats were prepared from the animal house of Baqiyatallah University of Medical Sciences and they were randomly divided into six groups including: 1) control, 2) exercise, 3) flax seed oil extract at 10mg/kg, 4) flax seed oil extract at dose of 30 mg/kg, 5) exercise with flax seed oil extract of 10 mg/kg, and 6) exercise with flax seed oil extract at a dose of 30 mg/kg [27].
To prepare flax seed oil, fresh flax seed was first prepared from Mehriz city of Yazd province. After drying, the oil was extracted and used in doses to be fed to rats. The groups 2, 5 and 6 did the exercises for 10 weeks and each week for five sessions including running with a 90-95% VO2max intensity (maximum oxygen consumption) on the treadmill for rodents on specific time during the day, and meanwhile the control group were placed on a treadmill at a speed of 2m/min for equalizing stress impact for 15 minutes. It should be noted that the HILT practice protocol included three stages of warm up, the body exercise (three intervals) and cooling down. The exercise in warm-up stage was 6 minute running with 50-60% VO2max intensity, the main body phase of 4-minute intense exercise with 90-95% vo2max, and low intense exercise for 2 minutes with 50-60% vo2 max intensity, and the cooling down stage included 6 minutes of 50-60% vo2max intensity. The training protocol lasted up to 72 hours before killing the rats. At the end of the study, the rats were killed and blood samples were taken directly from their hearts. After bleeding, the samples were centrifuged for 15 minutes at a speed of 3000rpm with centrifugal machines (Hitachi, Japan). For biochemical analysis and measurement of IL1β and TNF-α, Elisa commercial kits (Koma; Korea) and Elisa Reader (spectera, Austria) were used. All information was reported as mean. Shapiro-Wilk test was used to check the normal distribution of data and for comparison of serum levels of TNF-α and IL1β in the six groups, one-way ANOVA and LSD post-hoc test were used.
Serum levels of IL1β (F=3.56; p=0.01) and TNF-α (F=11.54; p=0.001) were significantly different in the six groups of rats that is the IL1β serum levels in the exercise groups (p=0.008), exercise with 10 mg/kg extract (p=0.01), and exercise with 30 mg/kg extract (p=0.001) were significantly lower than the control group, and in the exercise group with 30 mg/kg of the extract, they were significantly lower than flax seed extract group at a dose of 10mg/kg (p=0.01). Also, serum levels of TNF-α in the exercise groups (p=0.03), flax seed oil extract with dose of 30 mg/kg (p=0.02), exercise with flax seed oil extract with dose of 10 mg/kg (p=0.005) and exercise with flax seed oil extract with dose of 30 mg/kg (p=0.001) were significantly lower than the control group. Serum level of TNF-α with the flax seed oil extract at 30 mg/kg were significantly lower than the other groups (p=0.001; Table 1).
… [32-38]. In a study, the effect of 12 weeks training on cytokines activity was studied in 28 patients with coronary artery disease with the mean age of 64.00±7.10 years. The training program included 45 minutes of aerobic training with intensity of 70-80% HRmax for 12 weeks. The results of this study showed that aerobic training significantly reduced TNF-α, IL-1β, IL-6 and CRP [8]. Limited studies have been conducted on the simultaneous effect of HILT exercise and flaxseed supplementation on inflammatory factors. In a single study that was conducted in 2012 and the results of that study are consistent with the present study, it was found that the simultaneous effect of exercise and flax oil supplementation resulted in significant decrease in IL1β and TNF-α levels in ischemic rats [31]. It seems that high levels of these indices in ischemic rats are a reason for the meaningfulness of exercise and nutritional interventions, although the results are consistent with the present study. In general, many physiological and metabolic factors that affect metabolism include lower muscle mass, higher fat, different fat distribution, serum lipid levels, and other factors such as gender, health level, race, diet, weight, BMI (Body Mass Index), exercise intensity, exercise volume, exercise duration, exercise type, number of people, difference in energy expenditure, activity level outside the exercise program, and calorie intake can be effective on the wide range of TNF-α and IL1β inflammatory mediatory responses to the exercise [39, 40]. … [41-48].
It is suggested that intense aerobic exercises and flax seed oil supplementation simultaneously be used to prevent and treat cardiovascular disease.
Among the limitations of this study, lack of measurement of the caloric intake of subjects during exercise and the lack of control of injury of rats during severe aerobic exercises can be mentioned.
10 weeks of intense periodic exercises and flaxseed oil consumption have interactive effects in reducing the serum levels of TNF-α and IL-1β in rats.
We appreciate the financial and spiritual contribution of the Research Deputy of Islamic Azad University of Central Tehran Branch and Baqiyatallah University of Medical Sciences.
Non-declared
This research protocol was set based on international law on the protection of laboratory animals and it was approved by the Ethics Committee of the University.
This study is taken from PhD. Dissertation of Mr. Younes Khademi approved by Islamic Azad University of Central Tehran Branch with the guidance of Dr. Mohammad Ali Azarbayejani and consultation of Dr. Seyed Ali Hosseini.
TABLES and CHARTS
Show attach fileCITIATION LINKS
[1]Blake GJ, Ridker PM. Inflammatory bio-markers and cardiovascular risk prediction. J Int Med. 2002;252(4):283-94.
[2]Blake GJ, Ridker PM. Novel clinical markers of vascular wall inflammation. Circ Res. 2001;89 (9):763-71.
[3]Geffken DF, Cushman M, Burke GL, Polak JF, Sakkinen PA, Tracy RP. Association between physical activity and markers of inflammation in a healthy elderly population. Am J Epidemiol. 2001;153(3):242-50.
[4]Rohde LE, Hennekens CH, Ridker PM. Cross-sectional study of soluble intercellular adhesion molecule-1 and cardiovascular risk factors in apparently healthy men. Arterioscler Throm Vasc Biol. 1999;19(7):1595-9.
[5]Signorelli SS, Mazzarino MC, Di Pino L, Malaponte G, Porto C, Pennisi G, et al. High circulating levels of cytokines (IL-6 and TNFalpha), adhesion molecules (VCAM-1 and ICAM-1) and selectins in patients with peripheral arterial disease at rest and after a treadmill test. Vasc Med. 2003;8(1):15-9.
[6]Tousoulis D, Davies G, Stefanadis C, Toutouzas P, Ambrose JA. Inflammatory and thrombotic mechanisms in coronary atherosclerosis. Heart. 2003;89(9):993-7.
[7]Kargarfard M, Lam ET, Shariat A, Asle Mohammadi M, Afrasiabi S, Shaw I, et al. Effects of endurance and high intensity training on ICAM-1 and VCAM-1 levels and arterial pressure in obese and normal weight adolescents. Physsician Sportsmed. 2016;44(3):208-16.
[8]Goldhammer E, Tanchilevitch A, Maor I, Beniamini Y, Rosenschein U, Sagiv M. Exercise training modulates cytokines activity in coronary heart disease patients. Int J Cardiol. 2005;100(1):93-9.
[9]Nemet D, Hong S, Mills PJ, Ziegler MG, Hill M, Cooper DM. Systemic vs. local cytokine and leukocyte responses to unilateral wrist flexion exercise. J Appl Physiol. 2002;93(2):546-54.
[10]Ziccardi P, Nappo F, Giugliano G, Esposito K, Marfella R, Cioffi M, et al. Reduction of inflammatory cytokine concentrations and improvement of endothelial functions in obese women after weight loss over one year. Circulation. 2002;105(7):804-9.
[11]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.
[12]Nassis GP, Papantakou K, Skenderi K, Triandafillopoulou M, Kavouras SA, Yannakoulia M, et al. Aerobic exercise training improves insulin sensitivity without changes in body weight, body fat, adiponectin, and inflammatory markers in overweight and obese girls. Metabolism. 2005;54(11):1472- 9.
[13]Ding YH, Young CN, Luan X, Li J, Rafols JA, Clark JC, et al. Exercise preconditioning ameliorates inflammatory injury in ischemic rats during reperfusion. Acta Neuropathol. 2005;109(3):237-46.
[14]Wang RY, Yang YR, Yu SM. Protective effects of treadmill training on infarction in rats. Brain Res. 2001;922(1):140-3.
[15]Mogharnasi M, Gaeini A.A, Javadi E, Kordi MR, Ravasi AA, Sheikholeslami vatani D. The Effect Of Endurance Training On Inflammatory Biomarkers & Lipid Profiles in Wistar Rats. World J Sport Sci. 2009;2(2):82-8.
[16]Aviram M. Interaction of oxidized low density lipoprotein with macrophages in atherosclerosis, and the antiatherogenicity of antioxidants. Eur J Clin Chem Clin Biochem. 1996;34(8):599- 608.
[17]Farahpour M.R, Taghikhani H, Habibi M, Zandieh M.A. Wound healing activity of flaxseed linum usitatissimum L in rat. African J Pharm Pharm. 2011;5(21):2386-9.
[18]Zuk M, Kulma A, Dyminska L, Szoltysek K, Prescha A, Hanuza J, et al. Flavonoid engineering of flax potentiate its biotechnological application. BMC Biotechnol. 2011;11:10.
[19]Sneddon AA, Tsofliou F, Fyfe CL, Matheson I, Jackson DM, Horgan G, et al. Effect of a conjugated linoleic acid and omega-3 fatty acid mixture on body composition and adiponectin. Obesity. 2008;16(5):1019-24.
[20]Connor SL, Connor WE. Are fish oils beneficial in the prevention and treatment of coronary artery disease? Am J Clin Nutr. 1997;66(Suppl 4):1020S-31S.
[21]Romieu I, Garcia-Esteban R, Sunyer J, Rios C, Alcaraz-Zubeldia M, Velasco SR, et al. The effect of supplementation with omega-3 polyunsaturated fatty acids on markers of oxidative stress in elderly exposed to PM(2.5). Envir Health Perspect. 2008;116(9):1237-42.
[22]Deng Y, Zhang CH, Zhang HN. Effects of chaihu shugan powder on the behavior and expressions of BDNF and TrkB in the hippocampus, amygdala, and the frontal lobe in rat model of depression. Zhongguo Zhong Xi Yi Jie He Za Zhi. 2011;31(10):1373-8.
[23]Chytilova M, Mudronova D, Nemcova R, Gancarcikova S, Buleca V, Koscova J, et al. Anti-inflammatory and immunoregulatory effects of flax-seed oil and Lactobacillus plantarum - Biocenol LP96 in gnotobiotic pigs challenged with enterotoxigenic Escherichia coli. Res Vet Sci. 2013;95(1):103-9.
[24]Chytilova M, Nemcova R, Gancarcikova S, Mudronova D, Tkacikova L. Flax-seed oil and Lactobacillus plantarum supplementation modulate TLR and NF-kappaB gene expression in enterotoxigenic Escherichia coli challenged gnotobiotic pigs. Acta Vet Hung. 2014;62(4):463-72.
[25]Green AG. Genetic control of polyunsaturated fatty acid biosynthesis in flax (Linum usitatissimum) seed oil. Theor Appl Genet. 1986;72(5):654-61.
[26]Tanna IR, Aghera HB, Ashok BK, Chandola HM. Protective role of Ashwagandharishta and flax seed oil against maximal electroshock induced seizures in albino rats. Ayu. 2012;33(1):114-8.
[27]Tuluce Y, Ozkol H, Koyuncu I. Photoprotective effect of flax seed oil (Linum usitatissimum L.) against ultraviolet C-induced apoptosis and oxidative stress in rats. Toxicol Ind Health. 2012;28(2):99- 107.
[28]Williams D, Verghese M, Walker LT, Boateng J, Shackelford L, Chawan CB. Flax seed oil and flax seed meal reduce the formation of aberrant crypt foci (ACF) in azoxymethane-induced colon cancer in Fisher 344 male rats. Food Chem Toxicol. 2007;45(1):153-9.
[29]Mirfatahi M, Tabibi H, Nasrollahi A, Hedayati M, Taghizadeh M. Effect of flaxseed oil on serum systemic and vascular inflammation markers and oxidative stress in hemodialysis patients: a randomized controlled trial. Int Urol Nephrol. 2016;48(8):1335-41.
[30]Ren GY, Chen CY, Chen GC, Chen WG, Pan A, Pan C-W, et al. Effect of Flaxseed Intervention on Inflammatory Marker C-Reactive Protein: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Nutrients. 2016;8(3):136.
[31]Nounou HA, Deif MM, Shalaby MA. Effect of flaxseed supplementation and exercise training on lipid profile, oxidative stress and inflammation in rats with myocardial ischemia. Lipids Health Dis. 2012;11: 129.
[32]Burgomaster KA, Heigenhauser GJ, Gibala MJ. Effect of short-term sprint interval training on human skeletal muscle carbohydrate metabolism during exercise and time-trial performance. J Appl Physiol. 2006;100(6):2041-7.
[33]Burgomaster KA, Howarth KR, Phillips SM, Rakobowchuk M, Macdonald MJ, McGee SL, et al. Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J Physiol. 2008;586(1):151-60.
[34]Rodas G, Ventura JL, Cadefau JA, Cusso R, Parra J. A short training programme for the rapid improvement of both aerobic and anaerobic metabolism. Eur J Appl Physiol. 2000;82(5-6):480-6.
[35]Wenger HA, Bell GJ. The interactions of intensity, frequency and duration of exercise training in altering cardiorespiratory fitness. Sports Med. 1986;3(5):346-56.
[36]Wisloff U, Ellingsen O, Kemi OJ. High-intensity interval training to maximize cardiac benefits of exercise training? Exerc Sport Sci Rev. 2009;37(3):139-46.
[37]Whyte LJ, Gill JM, Cathcart AJ. Effect of 2 weeks of sprint interval training on health-related outcomes in sedentary overweight/obese men. Metabolism. 2010; 59(10):1421-8.
[38]Ciolac EG. High-intensity interval training and hypertension: maximizing the benefits of exercise?. Am J Cardiovasc Dis. 2012;2(2):102-10.
[39]Sanadgol N, Mostafaie A, Mansouri K, Bahrami G. Effect of palmitic acid and linoleic acid on expression of ICAM-1 and VCAM-1 in human bone marrow endothelial cells (HBMECs). Arch Med Sci. 2012;8(2):192-8.
[40]Papageorgiou N, Tousoulis D, Psaltopoulou T, Giolis A, Antoniades C, Tsiamis E, et al. Divergent anti-inflammatory effects of different oil acute consumption on healthy individuals. Eur J Clin Nutr. 2011;65(4):514-9.
[41]Han H, Yan P, Chen L, Luo C, Gao H, Deng Q, et al. Flaxseed oil containing α-linolenic acid ester of plant sterol improved atherosclerosis in apoe deficient mice. Oxid Med Cel Longev. 2015;2015:958217
[42]W, Esselman WJ, Jump DB, Busik JV. Anti-inflammatory effect of docosahexaenoic acid on cytokine-induced adhesion molecule expression in human retinal vascular endothelial cells. Invest Ophthalmol Vis Sci. 2005;46(11):4342-7.
[43]Wang TM, CJ, Lee TS, Chao HY, Wu WH, Hsieh SC, et al. Docosahexaenoic acid attenuates VCAM-1 expression and NF-kappaB activation in TNF-alpha-treated human aortic endothelial cells. J Nut Biochem. 2011;22(2):187-94.
[44]De Winther MP, Kanters E, Kraal G, Hofker MH. Nuclear factor kappaB signaling in atherogenesis. Arterioscler Thromb Vasc Biol. 2005;25(5):904-14.
[45]Jaudszus A, Krokowski M, Mockel P, Darcan Y, Avagyan A, Matricardi P, et al. Cis-9,trans-11-conjugated linoleic acid inhibits allergic sensitization and airway inflammation via a PPARgamma-related mechanism in mice. J Nutr. 2008;138(7):1336-42.
[46]Ridker PM, Hennekens CH, Buring JE, Rifai N. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med. 2000;342(12):836-43.
[47]Spittle MA, Hoenich NA, Handelman GJ, Adhikarla R, Homel P, Levin NW. Oxidative stress and inflammation in hemodialysis patients. Am J Kidney Dis. 2001;38(6):1408-13.
[48]Li H, Ruan XZ, Powis SH, Fernando R, Mon WY, Wheeler DC, et al. EPA and DHA reduce LPS-induced inflammation responses in HK-2 cells: evidence for a PPAR-gamma-dependent mechanism. Kidney Int. 2005;67(3):867-74.
[2]Blake GJ, Ridker PM. Novel clinical markers of vascular wall inflammation. Circ Res. 2001;89 (9):763-71.
[3]Geffken DF, Cushman M, Burke GL, Polak JF, Sakkinen PA, Tracy RP. Association between physical activity and markers of inflammation in a healthy elderly population. Am J Epidemiol. 2001;153(3):242-50.
[4]Rohde LE, Hennekens CH, Ridker PM. Cross-sectional study of soluble intercellular adhesion molecule-1 and cardiovascular risk factors in apparently healthy men. Arterioscler Throm Vasc Biol. 1999;19(7):1595-9.
[5]Signorelli SS, Mazzarino MC, Di Pino L, Malaponte G, Porto C, Pennisi G, et al. High circulating levels of cytokines (IL-6 and TNFalpha), adhesion molecules (VCAM-1 and ICAM-1) and selectins in patients with peripheral arterial disease at rest and after a treadmill test. Vasc Med. 2003;8(1):15-9.
[6]Tousoulis D, Davies G, Stefanadis C, Toutouzas P, Ambrose JA. Inflammatory and thrombotic mechanisms in coronary atherosclerosis. Heart. 2003;89(9):993-7.
[7]Kargarfard M, Lam ET, Shariat A, Asle Mohammadi M, Afrasiabi S, Shaw I, et al. Effects of endurance and high intensity training on ICAM-1 and VCAM-1 levels and arterial pressure in obese and normal weight adolescents. Physsician Sportsmed. 2016;44(3):208-16.
[8]Goldhammer E, Tanchilevitch A, Maor I, Beniamini Y, Rosenschein U, Sagiv M. Exercise training modulates cytokines activity in coronary heart disease patients. Int J Cardiol. 2005;100(1):93-9.
[9]Nemet D, Hong S, Mills PJ, Ziegler MG, Hill M, Cooper DM. Systemic vs. local cytokine and leukocyte responses to unilateral wrist flexion exercise. J Appl Physiol. 2002;93(2):546-54.
[10]Ziccardi P, Nappo F, Giugliano G, Esposito K, Marfella R, Cioffi M, et al. Reduction of inflammatory cytokine concentrations and improvement of endothelial functions in obese women after weight loss over one year. Circulation. 2002;105(7):804-9.
[11]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.
[12]Nassis GP, Papantakou K, Skenderi K, Triandafillopoulou M, Kavouras SA, Yannakoulia M, et al. Aerobic exercise training improves insulin sensitivity without changes in body weight, body fat, adiponectin, and inflammatory markers in overweight and obese girls. Metabolism. 2005;54(11):1472- 9.
[13]Ding YH, Young CN, Luan X, Li J, Rafols JA, Clark JC, et al. Exercise preconditioning ameliorates inflammatory injury in ischemic rats during reperfusion. Acta Neuropathol. 2005;109(3):237-46.
[14]Wang RY, Yang YR, Yu SM. Protective effects of treadmill training on infarction in rats. Brain Res. 2001;922(1):140-3.
[15]Mogharnasi M, Gaeini A.A, Javadi E, Kordi MR, Ravasi AA, Sheikholeslami vatani D. The Effect Of Endurance Training On Inflammatory Biomarkers & Lipid Profiles in Wistar Rats. World J Sport Sci. 2009;2(2):82-8.
[16]Aviram M. Interaction of oxidized low density lipoprotein with macrophages in atherosclerosis, and the antiatherogenicity of antioxidants. Eur J Clin Chem Clin Biochem. 1996;34(8):599- 608.
[17]Farahpour M.R, Taghikhani H, Habibi M, Zandieh M.A. Wound healing activity of flaxseed linum usitatissimum L in rat. African J Pharm Pharm. 2011;5(21):2386-9.
[18]Zuk M, Kulma A, Dyminska L, Szoltysek K, Prescha A, Hanuza J, et al. Flavonoid engineering of flax potentiate its biotechnological application. BMC Biotechnol. 2011;11:10.
[19]Sneddon AA, Tsofliou F, Fyfe CL, Matheson I, Jackson DM, Horgan G, et al. Effect of a conjugated linoleic acid and omega-3 fatty acid mixture on body composition and adiponectin. Obesity. 2008;16(5):1019-24.
[20]Connor SL, Connor WE. Are fish oils beneficial in the prevention and treatment of coronary artery disease? Am J Clin Nutr. 1997;66(Suppl 4):1020S-31S.
[21]Romieu I, Garcia-Esteban R, Sunyer J, Rios C, Alcaraz-Zubeldia M, Velasco SR, et al. The effect of supplementation with omega-3 polyunsaturated fatty acids on markers of oxidative stress in elderly exposed to PM(2.5). Envir Health Perspect. 2008;116(9):1237-42.
[22]Deng Y, Zhang CH, Zhang HN. Effects of chaihu shugan powder on the behavior and expressions of BDNF and TrkB in the hippocampus, amygdala, and the frontal lobe in rat model of depression. Zhongguo Zhong Xi Yi Jie He Za Zhi. 2011;31(10):1373-8.
[23]Chytilova M, Mudronova D, Nemcova R, Gancarcikova S, Buleca V, Koscova J, et al. Anti-inflammatory and immunoregulatory effects of flax-seed oil and Lactobacillus plantarum - Biocenol LP96 in gnotobiotic pigs challenged with enterotoxigenic Escherichia coli. Res Vet Sci. 2013;95(1):103-9.
[24]Chytilova M, Nemcova R, Gancarcikova S, Mudronova D, Tkacikova L. Flax-seed oil and Lactobacillus plantarum supplementation modulate TLR and NF-kappaB gene expression in enterotoxigenic Escherichia coli challenged gnotobiotic pigs. Acta Vet Hung. 2014;62(4):463-72.
[25]Green AG. Genetic control of polyunsaturated fatty acid biosynthesis in flax (Linum usitatissimum) seed oil. Theor Appl Genet. 1986;72(5):654-61.
[26]Tanna IR, Aghera HB, Ashok BK, Chandola HM. Protective role of Ashwagandharishta and flax seed oil against maximal electroshock induced seizures in albino rats. Ayu. 2012;33(1):114-8.
[27]Tuluce Y, Ozkol H, Koyuncu I. Photoprotective effect of flax seed oil (Linum usitatissimum L.) against ultraviolet C-induced apoptosis and oxidative stress in rats. Toxicol Ind Health. 2012;28(2):99- 107.
[28]Williams D, Verghese M, Walker LT, Boateng J, Shackelford L, Chawan CB. Flax seed oil and flax seed meal reduce the formation of aberrant crypt foci (ACF) in azoxymethane-induced colon cancer in Fisher 344 male rats. Food Chem Toxicol. 2007;45(1):153-9.
[29]Mirfatahi M, Tabibi H, Nasrollahi A, Hedayati M, Taghizadeh M. Effect of flaxseed oil on serum systemic and vascular inflammation markers and oxidative stress in hemodialysis patients: a randomized controlled trial. Int Urol Nephrol. 2016;48(8):1335-41.
[30]Ren GY, Chen CY, Chen GC, Chen WG, Pan A, Pan C-W, et al. Effect of Flaxseed Intervention on Inflammatory Marker C-Reactive Protein: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Nutrients. 2016;8(3):136.
[31]Nounou HA, Deif MM, Shalaby MA. Effect of flaxseed supplementation and exercise training on lipid profile, oxidative stress and inflammation in rats with myocardial ischemia. Lipids Health Dis. 2012;11: 129.
[32]Burgomaster KA, Heigenhauser GJ, Gibala MJ. Effect of short-term sprint interval training on human skeletal muscle carbohydrate metabolism during exercise and time-trial performance. J Appl Physiol. 2006;100(6):2041-7.
[33]Burgomaster KA, Howarth KR, Phillips SM, Rakobowchuk M, Macdonald MJ, McGee SL, et al. Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J Physiol. 2008;586(1):151-60.
[34]Rodas G, Ventura JL, Cadefau JA, Cusso R, Parra J. A short training programme for the rapid improvement of both aerobic and anaerobic metabolism. Eur J Appl Physiol. 2000;82(5-6):480-6.
[35]Wenger HA, Bell GJ. The interactions of intensity, frequency and duration of exercise training in altering cardiorespiratory fitness. Sports Med. 1986;3(5):346-56.
[36]Wisloff U, Ellingsen O, Kemi OJ. High-intensity interval training to maximize cardiac benefits of exercise training? Exerc Sport Sci Rev. 2009;37(3):139-46.
[37]Whyte LJ, Gill JM, Cathcart AJ. Effect of 2 weeks of sprint interval training on health-related outcomes in sedentary overweight/obese men. Metabolism. 2010; 59(10):1421-8.
[38]Ciolac EG. High-intensity interval training and hypertension: maximizing the benefits of exercise?. Am J Cardiovasc Dis. 2012;2(2):102-10.
[39]Sanadgol N, Mostafaie A, Mansouri K, Bahrami G. Effect of palmitic acid and linoleic acid on expression of ICAM-1 and VCAM-1 in human bone marrow endothelial cells (HBMECs). Arch Med Sci. 2012;8(2):192-8.
[40]Papageorgiou N, Tousoulis D, Psaltopoulou T, Giolis A, Antoniades C, Tsiamis E, et al. Divergent anti-inflammatory effects of different oil acute consumption on healthy individuals. Eur J Clin Nutr. 2011;65(4):514-9.
[41]Han H, Yan P, Chen L, Luo C, Gao H, Deng Q, et al. Flaxseed oil containing α-linolenic acid ester of plant sterol improved atherosclerosis in apoe deficient mice. Oxid Med Cel Longev. 2015;2015:958217
[42]W, Esselman WJ, Jump DB, Busik JV. Anti-inflammatory effect of docosahexaenoic acid on cytokine-induced adhesion molecule expression in human retinal vascular endothelial cells. Invest Ophthalmol Vis Sci. 2005;46(11):4342-7.
[43]Wang TM, CJ, Lee TS, Chao HY, Wu WH, Hsieh SC, et al. Docosahexaenoic acid attenuates VCAM-1 expression and NF-kappaB activation in TNF-alpha-treated human aortic endothelial cells. J Nut Biochem. 2011;22(2):187-94.
[44]De Winther MP, Kanters E, Kraal G, Hofker MH. Nuclear factor kappaB signaling in atherogenesis. Arterioscler Thromb Vasc Biol. 2005;25(5):904-14.
[45]Jaudszus A, Krokowski M, Mockel P, Darcan Y, Avagyan A, Matricardi P, et al. Cis-9,trans-11-conjugated linoleic acid inhibits allergic sensitization and airway inflammation via a PPARgamma-related mechanism in mice. J Nutr. 2008;138(7):1336-42.
[46]Ridker PM, Hennekens CH, Buring JE, Rifai N. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med. 2000;342(12):836-43.
[47]Spittle MA, Hoenich NA, Handelman GJ, Adhikarla R, Homel P, Levin NW. Oxidative stress and inflammation in hemodialysis patients. Am J Kidney Dis. 2001;38(6):1408-13.
[48]Li H, Ruan XZ, Powis SH, Fernando R, Mon WY, Wheeler DC, et al. EPA and DHA reduce LPS-induced inflammation responses in HK-2 cells: evidence for a PPAR-gamma-dependent mechanism. Kidney Int. 2005;67(3):867-74.