تاثیر تمرین تناوبی شدید و کورکومین بر محتوای کاسپاز 3 و بیان ژنی miR-30، miR-199a و miR-874 قلب موشهای در معرض آرسنیک

نوع مقاله : مقاله پژوهشی

نویسندگان

1 دانشجوی دکتری فیزیولوژی ورزشی، گروه تربیت بدنی، واحد تبریز، دانشگاه آزاد اسلامی، تبریز، ایران

2 استادیار، گروه تربیت بدنی، واحد تبریز، دانشگاه آزاد اسلامی، تبریز، ایران

3 دانشیار فیزیولوژی ورزشی، گروه تربیت بدنی، واحد تبریز، دانشگاه آزاد اسلامی، تبریز، ایران

4 استادیار، گروه دامپزشکی، واحد تبریز، دانشگاه آزاد اسلامی، تبریز، ایران

5 دانشیار، گروه فیزیولوژی ورزشی، دانشگاه شهید مدنی آذربایجان، تبریز، ایران

چکیده

هدف: مواجهه با ارسنیک منجر به آپوپتوز کاردیومیوسیتی و نارسایی قلبی می‌شود و به نظر می‌رسد که تمرین تناوبی شدید (HIIT) و کورکورمین بتواند در این زمینه کمک کننده باشد.

روش شناسی: تعداد 48 سر رت نر به شش گروه شامل آرسنیک-تمرین، آرسنیک-کورکومین، آرسنیک-توام(شامل آرسنیک-تمرین-کورکومین)، آرسنیک، کنترل اتانول و کنترل آب مقطر تقسیم‌ شدند. آرسنیک به مدت شش هفته روزانه 5 میلی‌گرم به ازای هر کیلوگرم وزن بدن و کورکومین روزانه 15 میلی‌گرم به ازای هر کیلوگرم وزن بدن به صورت گاواژ خوراکی استفاده شد. پروتکل تمرین ورزشی با شدت بالا به مدت شش هفته (، 5 روز در هفته) شامل 60 دقیقه دویدن تناوبی (4 دقیقه دویدن با شدت 90-85 درصد VO2max و 2 دقیقه ریکاوری فعال با شدت 60 – 50 درصد) انجام شد.

نتایج: مواجهه با آرسنیک در مقایسه با گروه کنترل سبب افزایش مقدار کاسپاز 3 (001/0=P) و کاهش بیان miR-30 (001/0=P) قلب شد که این تغییرات فقط با کورکومین جبران (به ترتیب 039/0=P و 003/0=P) شدند. ولی تمرین HIIT هم اثرات مواجهه با آرسنیک بر افزایش مقدار کاسپاز 3 و کاهش بیان miR-30 را (به ترتیب 095/0=P و 26/0=P) تشدید نکرد.

نتیجه‌گیری: مواجهه با آرسنیک احتمالا قلب را به سمت آپوپتوز سوق می‌دهد و تصور می شود که فقط مصرف کورکومین این روند را تقلیل می‌دهد. همچنین به نظر می رسد با اینکه تمرین HIIT قادر به فرونشاندن آثار سوء آرسنیک نیست، ولی آپوپتوز قلبی را تشدید نمی‌کند. بااینحال به دلیل کمبود شواهد و محدودیتهای زیاد، هنوز نیاز به تحقیقات بیشتری وجود دارد.

کلیدواژه‌ها

عنوان مقاله [English]

Effects of HIIT and curcumin on cardiac caspase 3 level and expression of miR-30, miR-199a and miR-874 in rats exposed to arsenic

نویسندگان [English]

  • Abolfazl Majidi 1
  • Roghayeh Poozesh Jadidi 2
  • Jabbar Bashiri 3
  • Mir Ali Reza Nourazar 4
  • Karim Azali Alamdari 5
1 PHD student of Exercise Physiology, Department of Physical Education, Tabriz
2 Assistant Prof., Department of Exercise Physiology, Tabriz branch, Islamic Azad University, Tabriz, Iran
3 Associate Prof., Department of Exercise Physiology, Tabriz branch, Islamic Azad University, Tabriz, Iran
4 Assistant Prof., Department of Vet, Tabriz branch, Islamic Azad University, Tabriz, Iran
5 Associate Professor of Exercise Physiology, Azarbaijan Shahid Madani University, Tabriz, Iran
چکیده [English]

Aim: Arsenic exposure leads to cardiomyocyte apoptosis as well as cardiac failure and it seems high intensity interval training (HIIT) and curcumin supplementation could be beneficial. However, no straight information is available in this area. Therefore, the effects of HIIT and curcumin supplementation on myocardial caspase 3 level as well as expression of miR-30, miR-199a and miR-874 were investigated in rats exposed to arsenic via drinking water.

Methods: 48 rats were randomized in six groups including Arsenic-training, Arsenic-curcumin, Arsenic-training+curcumin, arsenic, ethanol control and normal control. Arsenic 5 mg/bw.day and curcumin 15 mg/bw.day, were consumed orally for entire the study period. HIIT were conducted for six weeks (5 d/w, 60 min/session (with 4 min running at 85-90% of Vo2max and 2 min recovery at 50-60% of Vo2max intervals).

Results: Arsenic exposure increased cardiac caspase 3 level (P=0.001), while decreased mir-30 expression (P=0.001) compared to control group and these changes could only attenuated by curcumin supplementation (P=0.039 and P=0.003 respectively). However, HIIT did not exacerbate effects from arsenic exposure upon caspase3 up regulation as well as a diminished mir-30 expression level (P=0.095 and P=0.26 respectively).

Conclusion: Arsenic exposure could likely predisposes the heart toward apoptosis which seems could be attenuated only by curcumin supplementation. Moreover it seems that HIIT fails to overcome arsenic toxicity; neither exuberate cardiac apoptosis. However, more researches are warranted because of the lack of evidence and also study limitations.

کلیدواژه‌ها [English]

  • Arsenic
  • Apoptosis
  • Curcumin
  • cardiac tissue
  • HIIT

مراجع

  1. Alamolhodaei NS, Shirani K, Karimi G. Arsenic cardiotoxicity: an overview. Environmental toxicology and pharmacology. 2015;40(3):1005-14.
  2. Raghu KG, Cherian OL. Characterization of cytotoxicity induced by arsenic trioxide (a potent anti-APL drug) in rat cardiac myocytes. Journal of trace elements in medicine and biology : organ of the Society for Minerals and Trace Elements (GMS). 2009;23(1):61-8.
  3. Jing Y, Dai J, Chalmers-Redman RM, Tatton WG, Waxman S. Arsenic trioxide selectively induces acute promyelocytic leukemia cell apoptosis via a hydrogen peroxide-dependent pathway. Blood. 1999;94(6):2102-11.
  4. Davison K, Cote S, Mader S, Miller WH. Glutathione depletion overcomes resistance to arsenic trioxide in arsenic-resistant cell lines. Leukemia. 2003;17(5):931-40.
  5. Zhao X, Feng T, Chen H, Shan H, Zhang Y, Lu Y, et al. Arsenic trioxide-induced apoptosis in H9c2 cardiomyocytes: implications in cardiotoxicity. Basic & clinical pharmacology & toxicology. 2008;102(5):419-25.
  6. van Empel VP, Bertrand AT, Hofstra L, Crijns HJ, Doevendans PA, De Windt LJ. Myocyte apoptosis in heart failure. Cardiovascular research. 2005;67(1):21-9.
  7. Chiong M, Wang Z, Pedrozo Z, Cao D, Troncoso R, Ibacache M, et al. Cardiomyocyte death: mechanisms and translational implications. Cell death & disease. 2011;2(12):e244.
  8. Mani K. Programmed cell death in cardiac myocytes: strategies to maximize post-ischemic salvage. Heart failure reviews. 2008;13(2):193-209.
  9. Pahlavani HA, Veisi A. The effect of aerobic and anaerobic training with melatonin consumption on the expression of apoptotic genes BAX and BCL2 myocardial in rats after ischemic reperfusion. Journal of Human Sport and Exercise. 2018;1(1):454-66.
  10. Zhao Y-c. [Effects of exercise training on myocardial mitochondrial miR-499-CaN-Drp-1 apoptotic pathway in mice]. Zhongguo Ying Yong Sheng Li Xue Za Zhi. 2015;31(3):259-63.
  11. Rimbaud S, Garnier A, Ventura-Clapier R. Mitochondrial biogenesis in cardiac pathophysiology. Pharmacological Reports. 2009;61(1):131-8.
  12. Abel ED, Doenst T. Mitochondrial adaptations to physiological vs. pathological cardiac hypertrophy. Cardiovascular Research. 2011;90(2):234-42.
  13. Jiang H-K, Wang Y-H, Sun L, He X, Zhao M, Feng Z-H, et al. Aerobic interval training attenuates mitochondrial dysfunction in rats post-myocardial infarction: roles of mitochondrial network dynamics. International journal of molecular sciences. 2014;15(4):5304-22.
  14. Pace C, Dagda R, Angermann J. Antioxidants protect against arsenic induced mitochondrial cardio-toxicity. Toxics. 2017;5(4):38.
  15. Yadav RS, Sankhwar ML, Shukla RK, Chandra R, Pant AB, Islam F, et al. Attenuation of arsenic neurotoxicity by curcumin in rats. Toxicology and Applied Pharmacology. 2009;240(3):367-76.
  16. Shehzad A, Lee YS. Molecular mechanisms of curcumin action: Signal transduction. BioFactors. 2013;39(1):27-36.
  17. Williams AH, Liu N, Van Rooij E, Olson EN. MicroRNA control of muscle development and disease. Current opinion in cell biology. 2009;21(3):461-9.
  18. Li P. MicroRNAs in Cardiac Apoptosis. Journal of Cardiovascular Translational Research. 2010;3(3):219-24.
  19. Wang K, Liu F, Zhou LY, Ding SL, Long B, Liu CY, et al. miR-874 regulates myocardial necrosis by targeting caspase-8. Cell Death &Amp; Disease. 2013;4:e709.
  20. Li J, Donath S, Li Y, Qin D, Prabhakar BS, Li P. miR-30 regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway. PLoS genetics. 2010;6(1):e1000795-e.
  21. Cassidy-Stone A, Chipuk JE, Ingerman E, Song C, Yoo C, Kuwana T, et al. Chemical Inhibition of the Mitochondrial Division Dynamin Reveals Its Role in Bax/Bak-Dependent Mitochondrial Outer Membrane Permeabilization. Developmental Cell. 2008;14(2):193-204.
  22. Rane S, He M, Sayed D, Vashistha H, Malhotra A, Sadoshima J, et al. Downregulation of miR-199a derepresses hypoxia-inducible factor-1α and Sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes. Circulation research. 2009;104(7):879-86.
  23. Ren X, Gaile DP, Gong Z, Qiu W, Ge Y, Zhang C, et al. Arsenic responsive microRNAs in vivo and their potential involvement in arsenic-induced oxidative stress. Toxicology and applied pharmacology. 2015;283(3):198-209.
  24. Nam Y-J, Mani K, Wu L, Peng C-F, Calvert JW, Foo RS-Y, et al. The apoptosis inhibitor ARC undergoes Ubiquitin-Proteasomal-mediated degradation in response to death stimuli identification of a degradation-resistant mutant. Journal of Biological Chemistry. 2007;282(8):5522-8.
  25. Yurkova N, Shaw J, Blackie K, Weidman D, Jayas R, Flynn B, et al. The Cell Cycle Factor E2F-1 Activates Bnip3 and the Intrinsic Death Pathway in Ventricular Myocytes. Circulation Research. 2008;102(4):472-9.
  26. Long X, Boluyt MO, Hipolito ML, Lundberg MS, Zheng J-S, O'neill L, et al. p53 and the hypoxia-induced apoptosis of cultured neonatal rat cardiac myocytes. The Journal of clinical investigation. 1997;99(11):2635-43.
  27. Hemmati AA, Olapour S, Varzi HN, Khodayar MJ, Dianat M, Mohammadian B, et al. Ellagic acid protects against arsenic trioxide–induced cardiotoxicity in rat. Human & Experimental Toxicology. 2017;37(4):412-9.
  28. Biswas J, Roy S, Mukherjee S, Sinha D, Roy M. Indian spice curcumin may be an effective strategy to combat the genotoxicity of arsenic in Swiss albino mice. Asian Pacific journal of cancer prevention : APJCP. 2010;11(1):239-47.
  29. Kraljevic J, Marinovic J, Pravdic D, Zubin P, Dujic Z, Wisloff U, et al. Aerobic interval training attenuates remodelling and mitochondrial dysfunction in the post-infarction failing rat heart. Cardiovascular research. 2013;99(1):55-64.
  30. Waring CD, Vicinanza C, Papalamprou A, Smith AJ, Purushothaman S, Goldspink DF, et al. The adult heart responds to increased workload with physiologic hypertrophy, cardiac stem cell activation, and new myocyte formation. European heart journal. 2012;35(39):2722-31.
  31. Liou C-M, Tsai S-C, Kuo C-H, Ting H, Lee S-D. Cardiac Fas-Dependent and Mitochondria-Dependent Apoptosis after Chronic Cocaine Abuse. International Journal of Molecular Sciences. 2014;15(4):5988-6001.
  32. Ruíz-Vera T, Ochoa-Martínez ÁC, Zarazúa S, Carrizales-Yáñez L, Pérez-Maldonado IN. Circulating miRNA-126, -145 and -155 levels in Mexican women exposed to inorganic arsenic via drinking water. Environmental Toxicology and Pharmacology. 2019;67:79-86.
  33. Wu X-D, Zeng K, Liu W-L, Gao Y-G, Gong C-S, Zhang C-X, et al. Effect of aerobic exercise on miRNA-TLR4 signaling in atherosclerosis. 2014;35(04):344-50.
  34. Yan B, Wang H, Tan Y, Fu WJCTiMC. microRNAs in Cardiovascular Disease: Small Molecules but Big Roles. 2019;19(21):1918-47.
  35. Grimaldi V, De Pascale MR, Zullo A, Soricelli A, Infante T, Mancini FP, et al. Evidence of epigenetic tags in cardiac fibrosis. Journal of Cardiology. 2017;69(2):401-8.
  36. Zhang X, Dong S, Jia Q, Zhang A, Li Y, Zhu Y, et al. The microRNA in ventricular remodeling: the miR-30 family. Bioscience Reports. 2019;39(8).
  37. Duisters RF, Tijsen AJ, Schroen B, Leenders JJ, Lentink V, van der Made I, et al. miR-133 and miR-30 regulate connective tissue growth factor: implications for a role of microRNAs in myocardial matrix remodeling. 2009;104(2):170-8.
  38. Gambacciani C, Chiavacci E, Evangelista M, Vesentini N, Kusmic C, Pitto LJCR. P274miR-29 and miR-30 are involved in cardiac epigenetic reprogramming after myocardial infarction and ischemia. 2012;93(suppl_1).
  39. Wijnen WJ, van der Made I, van den Oever S, Hiller M, de Boer BA, Picavet DI, et al. Cardiomyocyte-Specific miRNA-30c Over-Expression Causes Dilated Cardiomyopathy. PLOS ONE. 2014;9(5):e96290.
  40. Beck R, Bommarito P, Douillet C, Kanke M, Del Razo LM, García-Vargas G, et al. Circulating miRNAs Associated with Arsenic Exposure. Environmental Science & Technology. 2018;52(24):14487-95.
  41. Sassi Y, Avramopoulos P, Ramanujam D, Grüter L, Werfel S, Giosele S, et al. Cardiac myocyte miR-29 promotes pathological remodeling of the heart by activating Wnt signaling. 2017;8(1):1-11.
  42. Kang C, Chung E, Diffee G, Ji LL. Exercise training attenuates aging-associated mitochondrial dysfunction in rat skeletal muscle: role of PGC-1α. Experimental gerontology. 2013;48(11):1343-50.
  43. Li Y, Sun X, Wang L, Zhou Z, Kang YJ. Myocardial toxicity of arsenic trioxide in a mouse model. Cardiovascular toxicology. 2002;2(1):63-73.
  44. Miao X, Tang Z, Wang Y, Su G, Sun W, Wei W, et al. Metallothionein prevention of arsenic trioxide-induced cardiac cell death is associated with its inhibition of mitogen-activated protein kinases activation in vitro and in vivo. Toxicology Letters. 2013;220(3):277-85.
  45. Miao X, Tang Z, Wang Y, Su G, Sun W, Wei W, et al. Metallothionein prevention of arsenic trioxide-induced cardiac cell death is associated with its inhibition of mitogen-activated protein kinases activation in vitro and in vivo. Toxicology letters. 2013;220(3):277-85.
  46. Zhang J, Sun G, Luo Y, Wang M, Wang W, Du Y, et al. Salvianolic Acid A Protects H9c2 Cells from Arsenic Trioxide-Induced Injury via Inhibition of the MAPK Signaling Pathway. Cellular Physiology and Biochemistry. 2017;41(5):1957-69.
  47. Davison K, Mann KK, Waxman S, Miller WH. JNK activation is a mediator of arsenic trioxide-induced apoptosis in acute promyelocytic leukemia cells. Blood. 2004;103(9):3496-502.
  48. Zhang J-Y, Sun G-B, Wang M, Liao P, Du Y-Y, Yang K, et al. Arsenic trioxide triggered calcium homeostasis imbalance and induced endoplasmic reticulum stress-mediated apoptosis in adult rat ventricular myocytes. Toxicology research. 2016;5(2):682-8.
  49. Afousi AG, Gaeini A, Rakhshan K, Naderi N, Azar AD, Aboutaleb N. Targeting necroptotic cell death pathway by high-intensity interval training (HIIT) decreases development of post-ischemic adverse remodelling after myocardial ischemia/reperfusion injury. Journal of cell communication and signaling. 2018:1-13.
  50. Ghajari H, Hosseini SA, Farsi S. The Effect of Endurance Training Along with Cadmium Consumption on Bcl-2 and Bax Gene Expressions in Heart Tissue of Rats. Annals of Military and Health Sciences Research. 2019;17(1).
  51. Jafari A, Pourrazi H, Nikookheslat S, Baradaran B. Effect of exercise training on Bcl-2 and bax gene expression in the rat heart. Gene, Cell and Tissue. 2015;2(4):e60174.
  52. Alihemmati A, Ebadi F, Moghadaszadeh M, Asadi M, Zare P, Badalzadeh R. Effects of high-intensity interval training on the expression of microRNA-499 and pro-and anti-apoptotic genes in doxorubicin-cardiotoxicity in rats. Journal of Electrocardiology. 2019.
  53. Yi-Yuan L, Chen J-S, Wu X-B, Shyu W-C, Chaunchaiyakul R, Xian-Li Z, et al. Combined effects of 17β-estradiol and exercise training on cardiac apoptosis in ovariectomized rats. PLoS One. 2018;13(12):e0208633.
  54. Jazi AA, Abdi H, Shamsaei N, Khaksari M. Combination of atorvastatin–endurance training has positive effect on apoptosis and protein expression of sdf-1α/cxcr4 axis after myocardial infarction in rat's heart tissue. International Journal of Health Studies. 2017;3(2).
  55. Zhao Y. Effects of exercise training on myocardial mitochondrial miR-499-CaN-Drp-1 apoptotic pathway in mice. Zhongguo ying yong sheng li xue za zhi= Zhongguo yingyong shenglixue zazhi= Chinese journal of applied physiology. 2015;31(3):259.
  56. Zhao Y, Fu J, Gao B. Effects of different intensity exercise training on apoptosis-related microRNAs and the targeted proteins in cardiomyocytes. Zhongguo ying yong sheng li xue za zhi= Zhongguo yingyong shenglixue zazhi= Chinese journal of applied physiology. 2018;34(1):93-6.
  57. Lu K, Wang L, Wang C, Yang Y, Hu D, Ding R. Effects of high-intensity interval versus continuous moderate-intensity aerobic exercise on apoptosis, oxidative stress and metabolism of the infarcted myocardium in a rat model. Molecular medicine reports. 2015;12(2):2374.
  58. Yadav A, Lomash V, Samim M, Flora SJS. Curcumin encapsulated in chitosan nanoparticles: A novel strategy for the treatment of arsenic toxicity. Chemico-Biological Interactions. 2012;199(1):49-61.
  59. Yu S, Wang X, He X, Wang Y, Gao S, Ren L, et al. Curcumin exerts anti-inflammatory and antioxidative properties in 1-methyl-4-phenylpyridinium ion (MPP+)-stimulated mesencephalic astrocytes by interference with TLR4 and downstream signaling pathway. Cell Stress and Chaperones. 2016;21(4):697-705.
  60. Yeh C-H, Chen T-P, Wu Y-C, Lin Y-M, Jing Lin P. Inhibition of NFκB Activation with Curcumin Attenuates Plasma Inflammatory Cytokines Surge and Cardiomyocytic Apoptosis Following Cardiac Ischemia/Reperfusion1. Journal of Surgical Research. 2005;125(1):109-16.
  61. Kim YS, Kwon JS, Cho YK, Jeong MH, Cho JG, Park JC, et al. Curcumin reduces the cardiac ischemia–reperfusion injury: involvement of the toll-like receptor 2 in cardiomyocytes. The Journal of Nutritional Biochemistry. 2012;23(11):1514-23.
  62. Katamura M, Iwai-Kanai E, Nakaoka M, Okawa Y, Ariyoshi M. Curcumin attenuates doxorubicin-induced cardiotoxicity by inducing autophagy via the regulation of JNK phosphorylation. J Clin Exp Cardiol. 2014;5(1):337-48.
  63. Yang K, Xu C, Li X, Jiang H. Combination of D942 with curcumin protects cardiomyocytes from ischemic damage through promoting autophagy. Journal of cardiovascular pharmacology and therapeutics. 2013;18(6):570-81.
  64. Hosseinzadeh L, Behravan J, Mosaffa F, Bahrami G, Bahrami A, Karimi G. Curcumin potentiates doxorubicin-induced apoptosis in H9c2 cardiac muscle cells through generation of reactive oxygen species. Food and Chemical Toxicology. 2011;49(5):1102-9.
  65. Yang Y, Duan W, Lin Y, Yi W, Liang Z, Yan J, et al. SIRT1 activation by curcumin pretreatment attenuates mitochondrial oxidative damage induced by myocardial ischemia reperfusion injury. Free Radical Biology and Medicine. 2013;65:667-79.
  66. Morimoto T, Sunagawa Y, Fujita M, Hasegaswa K. Novel heart failure therapy targeting transcriptional pathway in cardiomyocytes by a natural compound, curcumin. Circulation journal. 2010;74(6):1059=67.
  67. Junkun L, Erfu C, Tony H, Xin L, Sudeep K, Mingliang Z, et al. Curcumin downregulates phosphate carrier and protects against doxorubicin induced cardiomyocyte apoptosis. BioMed research international. 2016;2016(1):1-6.
  68. Kohli S, Chhabra A, Jaiswal A, Rustagi Y, Sharma M, Rani V. Curcumin suppresses gelatinase B mediated norepinephrine induced stress in H9c2 cardiomyocytes. PloS one. 2013;8(10):e76519-e26.
  69. Kang BY, Khan JA, Ryu S, Shekhar R, Seung KB, Mehta JL. Curcumin reduces angiotensin II-mediated cardiomyocyte growth via LOX-1 inhibition. Journal of cardiovascular pharmacology. 2010;55(2):176-83.
  70. Morimoto T, Sunagawa Y, Kawamura T, Takaya T, Wada H, Nagasawa A, et al. The dietary compound curcumin inhibits p300 histone acetyltransferase activity and prevents heart failure in rats. The Journal of clinical investigation. 2008;118(3):868-78.
  71. Fiorillo C, Becatti M, Pensalfini A, Cecchi C, Lanzilao L, Donzelli G, et al. Curcumin protects cardiac cells against ischemia-reperfusion injury: effects on oxidative stress, NF-κB, and JNK pathways. Free Radical Biology and Medicine. 2008;45(6):839-46.
  72. Pan Y, Wang Y, Zhao Y, Peng K, Li W, Wang Y, et al. Inhibition of JNK phosphorylation by a novel curcumin analog prevents high glucose-induced inflammation and apoptosis in cardiomyocytes and the development of diabetic cardiomyopathy. Diabetes. 2014;63(10):3497-511.
  73. Yang X, Jiang H, Shi Y. Upregulation of heme oxygenase-1 expression by curcumin conferring protection from hydrogen peroxide-induced apoptosis in H9c2 cardiomyoblasts. Cell & bioscience. 2017;7(20):46-56.
  74. Rauf A, Imran M, Orhan IE, Bawazeer S. Health perspectives of a bioactive compound curcumin: A review. Trends in Food Science & Technology. 2018;74:33-45.
  75. Lee S-W, Nah S-S, Byon J-S, Ko HJ, Park S-H, Lee S-J, et al. Transient complete atrioventricular block associated with curcumin intake. International Journal of Cardiology. 2011;150(2):e50-e2.
  76. Pichler G, Grau-Perez M, Tellez-Plaza M, Umans J, Best L, Cole S, et al. Association of Arsenic Exposure With Cardiac Geometry and Left Ventricular Function in Young Adults. Circulation Cardiovascular imaging. 2019;12(5):e009018.
  77. Chowdhury R, van Daalen K. Arsenic: A Metal That Might Break Your Heart. Lippincott Williams & Wilkins TWO COMMERCE SQ, 2001 MARKET ST, PHILADELPHIA …; 2019.

 

پژوهش های فیزیولوژی و مدیریت در ورزش
دوره 14، شماره 1
خرداد 1401
صفحه 25-42

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