The effect of cold water immersion after eccentric exercise on antioxidant and oxidative markers in the skeletal muscle of male rats

Document Type : Original Article

Authors

1 Department of Sport Physiology, Faculty of Sport Sciences, Shahid Chamran University of Ahvaz, Ahvaz, Iran

2 Department of Basic Sciences, Division of Biochemistry and Molecular Biology, Faculty of Veterinary Medicine, Shahid Chamran University of Ahvaz, Ahvaz, Iran

Abstract

Background and Purpose: The balance between antioxidant and oxidative systems in skeletal muscle is crucial for maintaining both health and sports performance. Cold water immersion (CWI) as a recovery method may help in improving the performance of these systems and reduce the damage caused by oxidative stress. This study aimed to investigate the effect of cold water immersion after eccentric exercise (ECC) on antioxidant and oxidant indices in the skeletal muscle of rats.
Materials and Methods: Twenty-five male Wistar rats (12 weeks old; weight, 230±5 g) were randomly divided into control, Eccentric + PR (passive recovery), Eccentric + CWI, Eccentric + NWI (normal water immersion), and Eccentric + AR (active recovery) groups. The Eccentric exercise consisted of 90 min of downhill running on a treadmill with a speed of 16 m/min and -16° incline. For an active recovery, after eccentric exercise, rats ran on a treadmill for 10 min at a speed of 12 m/min on a flat surface. For the normal water immersion and cold water immersion protocols, after eccentric exercise the entire body of rats (excluding the head of animals) was immersed in plastic containers containing normal water at 25°C or cold water at 10°C for 10 minutes. One day after eccentric exercise, the animals were euthanized by peritoneal injection of ketamine + xylazine (10+100mg/kg) and their soleus muscles were removed under sterile conditions and transferred into a -70 °C freezer.
Results: Eccentric + Passive recovery significantly (p<0.05) reduced antioxidant indices including total antioxidant capacity (TAC), glutathione peroxidase (GPX), glutathione reductase (GR), and glutathione (GSH) compared to the control group. It also caused a significant (p<0.05) increase in oxidant indices including total oxidant status (TOS), oxidative stress index (OSI), and oxidized glutathione (GSSG). There was no significant differences between recovery methods after eccentric exercise (cold water immersion, normal water immersion, active recovery) in terms of antioxidant levels (GPX, glutathione S-transferase (GST), and GR) and oxidant levels (GSSG and glutathione ratio reduced to oxidized (GSH/GSSG)) compared to passive recovery (p>0.05). Despite this, cold water immersion significantly (p<0.05) increased antioxidant indices (GSH and TAC) and decreased oxidant indices (TOS and OSI) compared to passive recovery.
Conclusion: The results of this study demonstrated that eccentric exercise has a significant negative impact on the antioxidant and oxidative status of skeletal muscle and cold water immersion reduced oxidative stress and improved antioxidant status after eccentric exercise.

Keywords

Main Subjects

References

1-Afzalpour ME, Saghebjoo M, Zarban A, Jani M. Comparison of the effects of an acute resistance and aerobic exercise session on the antioxidant defense system and lipid peroxidation of healthy young men. Journal of Sport in Biomotor Sciences. 2013;6(2):39-50. [In Persian]
2- Halliwell B, Gutteridge JM. Free radicals in biology and medicine. Oxford university press, USA; 2015. Doi: 10.1093/acprof:oso/9780198717478.001.0001.
3- Lu SC. Glutathione synthesis. Biochimica et Biophysica Acta (BBA)-General Subjects. 2013 May
1;1830(5):3143-53. Doi: 10.1016/j.bbagen.2012.09.008.
4- Meister A. Glutathione-ascorbic acid antioxidant system in animals. The Journal of Biological Chemistry. 1994; 269(13), 9397-9400. Doi: 10.1016/s0021-9258(17)36891-6.
5- Maes M, Fišar Z, Medina M, Scapagnini G, Nowak G, Berk M. New drug targets in depression: inflammatory, cell-mediated immune, oxidative and nitrosative stress, mitochondrial, antioxidant, and neuroprogressive pathways. And new drug candidates—Nrf2 activators and GSK-3 inhibitors. Inflammopharmacology. 2012 Jun;20:127-50. . Doi: 10.1007/s10787-011-0111-7.
6- Maes M, Galecki P, Chang YS, Berk M. A review on the oxidative and nitrosative stress (O&NS) pathways in major depression and their possible contribution to the (neuro) degenerative processes in that illness. Progress in Neuro-Psychopharmacology and Biological Psychiatry. 2011 Apr 29;35(3):676-92. Doi: 10.1016/j.pnpbp.2010.05.004.
7- Erel O. A new automated colorimetric method for measuring total oxidant status. Clinical biochemistry. 2005 Dec 1;38(12):1103-11.  Doi:10.1016/j.clinbiochem.2005.08.008.
8- Cekici A, Kantarci A, Hasturk H, Van Dyke TE. Inflammatory and immune pathways in the pathogenesis of periodontal disease. Periodontology 2000. 2014 Feb;64(1):57-80. Doi:10.1111/prd.12002.
9- Fatouros IG, Chatzinikolaou A, Douroudos II, Nikolaidis MG, Kyparos A, Margonis K, Michailidis Y, Vantarakis A, Taxildaris K, Katrabasas I, Mandalidis D. Time-course of changes in oxidative stress and antioxidant status responses following a soccer game. The Journal of Strength & Conditioning Research. 2010 Dec 1;24(12):3278-86. Doi:10.1519/JSC.0b013e3181b60444
10- Barnett A. Using recovery modalities between training sessions in elite athletes: does it help?. Sports medicine. 2006 Sep;36:781-96. Doi:10.2165/00007256-200636090-00005.
11- Soligard T, Schwellnus M, Alonso JM, Bahr R, Clarsen B, Dijkstra HP, Gabbett T, Gleeson M, Hägglund M, Hutchinson MR, Van Rensburg CJ. How much is too much?(Part 1) International Olympic Committee consensus statement on load in sport and risk of injury. British journal of sports medicine. 2016 Sep 1;50(17):1030-41. Doi:10.1136/bjsports-2016-096581.
12- Meeusen R, Duclos M, Foster C, Fry A, Gleeson M, Nieman D, Raglin J, Rietjens G, Steinacker J, Urhausen A. Prevention, diagnosis, and treatment of the overtraining syndrome: joint consensus statement of the European College of Sport Science and the American College of Sports Medicine. Medicine and science in sports and exercise. 2013 Jan 1;45(1):186-205. Doi:10.1249/mss.0b013e318279a10a .
13- Bangsbo J. Performance in sports–With specific emphasis on the effect of intensified training. Scandinavian journal of medicine & science in sports. 2015 Dec;25:88-99. Doi:10.1111/sms.12605.
14- Mäkinen TM. Human cold exposure, adaptation, and performance in high latitude environments. American Journal of Human Biology: The Official Journal of the Human Biology Association. 2007 Mar;19(2):155-64. Doi: 10.1111/sms.12605.
15- Vieira A, Siqueira AF, Ferreira-Júnior JB, Do Carmo J, Durigan JL, Blazevich A, Bottaro M. The effect of water temperature during cold-water immersion on recovery from exercise-induced muscle damage. International journal of sports medicine. 2016 Aug 24:937-43. Doi:10.1055/s-0042-111438
16- Sutkowy P, Woźniak A, Boraczyński T, Mila-Kierzenkowska C, Boraczyński M. Postexercise Impact of Ice‐Cold Water Bath on the Oxidant‐Antioxidant Balance in Healthy Men. BioMed research international. 2015;2015(1):706141. Doi: 10.1155/2015/706141.
17- Pournot H, Bieuzen F, Duffield R, Lepretre PM, Cozzolino C, Hausswirth C. Short term effects of various water immersions on recovery from exhaustive intermittent exercise. European journal of applied physiology. 2011 Jul;111:1287-95. Doi: 10.1007/s00421-010-1754-6.
18- Ascensão A, Leite M, Rebelo AN, Magalhäes S, Magalhäes J. Effects of cold water immersion on the recovery of physical performance and muscle damage following a one-off soccer match. Journal of sports sciences. 2011 Feb 1;29(3):217-25. Doi:10.1080/02640414.2010.526132.
19- Augustyniak A, Skrzydlewska E. Zdolności antyoksydacyjne w starzejącym się organizmie Antioxidative abilities during aging. Postepy Hig Med Dosw (Online). 2004;58:194-201.
20- Proske U, Allen TJ. Damage to skeletal muscle from eccentric exercise. Exercise and sport sciences reviews. 2005 Apr 1;33(2):98-104.‌ Doi:10.1097/00003677-200504000-00007.
21- Jamurtas AZ, Fatouros IG. Eccentric exercise, muscle damage and oxidative stress. INTECH Open Access Publisher; 2012 Feb 17. Doi:10.5772/28588.
22- Klarod K, Surakul P. Mechanism of muscle injury from eccentric exercise induced free radicals and protection with antioxidants (P. 347). Chulalongkorn Medical Journal. 2020;64(3):347-54. Doi:10.58837/CHULA.CMJ.64.3.14.
23- Silva LA, Bom KF, Tromm CB, Rosa GL, Mariano I, Pozzi BG, Tuon T, Stresck EL, Souza CT, Pinho RA. Effect of eccentric training on mitochondrial function and oxidative stress in the skeletal muscle of rats. Brazilian Journal of Medical and Biological Research. 2013 Jan 11;46(1):14-20. Doi:10.1590/1414-431X20121956 .
24- Close GL, Ashton T, Cable T, Doran D, Holloway C, McArdle F, MacLaren DP. Ascorbic acid supplementation does not attenuate post-exercise muscle soreness following muscle-damaging exercise but may delay the recovery process. British Journal of Nutrition. 2006 May;95(5):976-81. Doi:10.1079/BJN20061732.
25- Ji LL, Leeuwenburgh C, Leichtweis S, Gore M, Fiebig R, Hollander J, Bejma J. Oxidative stress and aging: role of exercise and its influences on antioxidant systems. Annals of the New York Academy of Sciences. 1998 Nov;854(1):102-17. Doi:10.1111/j.1749-6632.1998.tb09896.x
26- Gunduz Fİ, Senturk UK, Kuru O, Aktekin B, Aktekin MR. The effect of one year swimming exercise on oxidant stress and antioxidant capacity in aged rats. Physiological Research. 2004 Jan 1;53(2):171-6. Doi:10.33549/physiolres.930384.
27- Lubkowska A, Dołęgowska B, Szyguła Z. Whole-body cryostimulation-potential beneficial treatment for improving antioxidant capacity in healthy men-significance of the number of sessions. Plos One. 2012;7(10):43-52. Doi:10.1371/journal.pone.0046352.
28- Lubkowska A, Dudzińska W, Bryczkowska I, Dołęgowska B. Body composition, lipid profile, adipokine concentration, and antioxidant capacity changes during interventions to treat overweight with exercise Programme and whole‐body Cryostimulation. Oxidative medicine and cellular longevity. 2015;2015(1):803197. Doi:10.1155/2015/803197.
29- Mila-Kierzenkowska C, Woźniak A, Szpinda M, Boraczyński T, Woźniak B, Rajewski P, Sutkowy P. Effects of thermal stress on the activity of selected lysosomal enzymes in blood of experienced and novice winter swimmers. Scandinavian Journal of Clinical and Laboratory Investigation. 2012 Dec 1;72(8):635-41.  Doi:10.3109/00365513.2012.727214.
30- Qun Z, Xinkai Y, Jing W. Effects of eccentric exercise on branched‐chain amino acid profiles in rat serum and skeletal muscle. Journal of animal physiology and animal nutrition. 2014 Apr;98(2):215-22. Doi: 10.1111/jpn.12062.
31- Camargo MZ, Siqueira CP, Preti MC, Nakamura FY, de Lima FM, Dias IF, Toginho Filho DD, Ramos SD. Effects of light emitting diode (LED) therapy and cold water immersion therapy on exercise-induced muscle damage in rats. Lasers in medical science. 2012 Sep;27:1051-8. . Doi: 10.1007/s10103-011-1039-2.
32- Spanidis Y, Veskoukis AS, Papanikolaou C, Stagos D, Priftis A, Deli CK, Jamurtas AZ, Kouretas D. Exercise‐induced reductive stress is a protective mechanism against oxidative stress in peripheral blood mononuclear cells. Oxidative Medicine and Cellular Longevity. 2018;2018(1):3053704. Doi: 10.1155/2018/3053704.
33- Ihsan M, Watson G, Abbiss CR. What are the physiological mechanisms for post-exercise cold water immersion in the recovery from prolonged endurance and intermittent exercise?. Sports Medicine. 2016 Aug;46:1095-109. Doi:10.1007/s40279-016-0483-3.
34- González D, Marquina R, Rondón N, Rodríguez-Malaver AJ, Reyes R. Effects of aerobic exercise on uric acid, total antioxidant activity, oxidative stress, and nitric oxide in human saliva. Research in Sports Medicine. 2008 Jun 12;16(2):128-37. Doi:10.1080/15438620802103700.
35- Watson TA, MacDonald-Wicks LK, Garg ML. Oxidative stress and antioxidants in athletes undertaking regular exercise training. International journal of sport nutrition and exercise metabolism. 2005 Apr 1;15(2):131-46. Doi:10.1123/ijsnem.15.2.131.
36- Rodrigo L, Hernández AF, López-Caballero JJ, Gil F, Pla A. Immunohistochemical evidence for the expression and induction of paraoxonase in rat liver, kidney, lung and brain tissue. Implications for its physiological role. Chemico-biological interactions. 2001 Aug 31;137(2):123-37.Doi:10.1016/s0009-2797(01)00225-3
37- White A, Estrada M, Walker K, Wisnia P, Filgueira G, Valdés F, Araneda O, Behn C, Martı́nez R. Role of exercise and ascorbate on plasma antioxidant capacity in thoroughbred race horses. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 2001 Jan 1;128(1):99-104. Doi:10.1016/S1095-6433(00)00286-5.
38- Bogdanis GC, Stavrinou P, Fatouros IG, Philippou A, Chatzinikolaou A, Draganidis D, Ermidis G, Maridaki M. Short-term high-intensity interval exercise training attenuates oxidative stress responses and improves antioxidant status in healthy humans. Food and Chemical Toxicology. 2013 Nov 1;61:171-7.  Doi:10.1016/j.fct.2013.05.046.
39- Hanachi P, Shemshaki A, Norouziyan S. The effect of eccentric exercise on total anti-oxidant capacity, reduced glutathione and malondialdehyde levels in active women. Zahedan Journal of Research in Medical Sciences. 2014;16(6). [In Persian]
40- Ficicilar H, Zergeroglu AM, Ersoz G, Erdogan A, Ozdemir S, Tekin D. The effects of short-term training on platelet functions and total antioxidant capacity in rats. Physiological research. 2006 Jan 1;55(2):151. Doi:10.33549/physiolres.930756
41- Afzalpour ME, Gharakhanlou R, Gaeini AA, Mohebbi H, Hedayati M, Khazaei M. The effects of aerobic exercises on the serum oxidized LDL and total antioxidant capacity in non-active men. CVD prevention and control. 2008 Apr 1;3(2):77-82. Doi:10.1016/j.cvdpc.2008.01.002.
42- Aguiló A, Tauler P, Fuentespina E, Tur JA, Córdova A, Pons A. Antioxidant response to oxidative stress induced by exhaustive exercise. Physiology & behavior. 2005 Jan 31;84(1):1-7. Doi:10.1016/j.physbeh.2004.07.034.
43- Elosua R, Molina L, Fito M, Arquer A, Sanchez-Quesada JL, Covas MI, Ordonez-Llanos J, Marrugat J. Response of oxidative stress biomarkers to a 16-week aerobic physical activity program, and to acute physical activity, in healthy young men and women. Atherosclerosis. 2003 Apr 1;167(2):327-34. Doi:10.1016/S0021-9150(03)00018-2
44- Kanter MM, Hamlin RL, Unverferth DV, Davis HW, Merola AJ. Effect of exercise training on antioxidant enzymes and cardiotoxicity of doxorubicin. Journal of applied physiology. 1985 Oct 1;59(4):1298-303. Doi:10.1152/jappl.1985.59.4.1298.
45- Dekany M, Nemeskeri V, Györe I, Harbula I, Malomsoki J, Pucsok J. Antioxidant status of interval-trained athletes in various sports. International journal of sports medicine. 2006 Feb;27(02):112-6. Doi:10.1055/s-2005-865634
46- Hiromi Miyazaki, Shuji oh-ishi, Takako Oakawara, Takako Kizaki, Koji Toshinai, Sung Ha, Shukoh Haga, Lili Ji and Hideki ohno, 2001. Strenuous endurance training in humans reduce oxidative stress following exhausting exercise. Eur. J. Appl. Hpysiol., 84: 1-2. Doi:10.1007/s004210000342.
47- Fisher-Wellman K, Bloomer RJ. Acute exercise and oxidative stress: a 30 year history. Dynamic medicine. 2009 Dec;8:1-25. Doi:10.1186/1476-5918-8-1.
48- Ohtsuka Y, Yabunaka N, Fujisawa H, Watanabe I, Agishi Y. Effect of thermal stress on glutathione metabolism in human erythrocytes. European journal of applied physiology and occupational physiology. 1994 Jan;68:87-91. Doi:10.1007/BF00599247.
49- Kaushik S, Kaur J. Chronic cold exposure affects the antioxidant defense system in various rat tissues. Clinica Chimica Acta. 2003 Jul 1;333(1):69-77. Doi:10.1016/S0009-8981(03)00171-2.
50- Ohno H, Kondo T, Fujiwara Y, Tagami SI, Kuroshima A, Kawakami Y. Effects of cold stress on glutathione and related enzymes in rat erythrocytes. International journal of biometeorology. 1991 Jun;35:111-3. Doi:10.1007/BF01087487.
51- Park EH, Choi SW, Yang YK. Cold-water immersion promotes antioxidant enzyme activation in elite taekwondo athletes. Applied Sciences. 2021 Mar 23;11(6):2855. Doi:10.3390/app11062855.
52- Wozniak A, Mila-Kierzenkowska C, Szpinda M, Chwalbinska-Moneta J, Augustynska B, Jurecka A. Whole-body cryostimulation and oxidative stress in rowers: the preliminary results. Archives of medical science: AMS. 2013 Apr 4;9(2):303. Doi:10.5114/aoms.2012.30835.
53- Bruunsgaard H, Galbo H, Halkjaer-Kristensen J, Johansen TL, MacLean DA, Pedersen BK. Exercise‐induced increase in serum interleukin‐6 in humans is related to muscle damage. The Journal of physiology. 1997 Mar 15;499(3):833-41. Doi:10.1113/jphysiol.1997.sp021972.
54- Seifi-Skishahr F, Damirchi A, Farjaminezhad M, Babaei P. Physical training status determines oxidative stress and redox changes in response to an acute aerobic exercise. Biochemistry Research International. 2016;2016(1):3757623. Doi:10.1155/2016/3757623.
55- Unt E, Kairane C, Vaher I, Zilmer M. Red blood cell and whole blood glutathione redox status in endurance-trained men following a ski marathon. Journal of sports science & medicine. 2008 Sep;7(3):344.
56- Elokda AS, Shields RK, Nielsen DH. Effects of a maximal graded exercise test on glutathione as a marker of acute oxidative stress. Journal of Cardiopulmonary Rehabilitation and Prevention. 2005 Jul 1;25(4):215-9. Doi:10.1097/00008483-200507000-00007.
57- Gohil KI, Viguie CH, Stanley WC, Brooks GA, Packer LE. Blood glutathione oxidation during human exercise. Journal of Applied Physiology. 1988 Jan 1;64(1):115-9. Doi:10.1152/jappl.1988.64.1.115.
58- Laires MJ, Madeira F, Sergio J, Colaco C, Vaz C, Felisberto GM, Neto I, Breitenfeld L, Bicho M, Manso C. Preliminary study of the relationship between plasma and erythrocyte magnesium variations and some circulating pro-oxidant and antioxidant indices in a standardized physical effort. Magnesium Research. 1993 Sep 1;6(3):233-8. Doi:10.1042/cs087s078.
59- Kretzschmar M, Müller D, Hübscher J, Marin E, Klinger W. Influence of aging, training and acute physical exercise on plasma glutathione and lipid peroxides in man. International journal of sports medicine. 1991 Apr;12(02):218-22. Doi:10.1055/s-2007-1024671.
60- Nikolaidis MG, Kyparos A, Hadziioannou M, Panou N, Samaras L, Jamurtas AZ, Kouretas D. Acute exercise markedly increases blood oxidative stress in boys and girls. Applied physiology, nutrition, and metabolism. 2007 Apr;32(2):197-205. Doi:10.1139/h06-097.
61- Barja de Quiroga G, Lopez-Torres M, Pérez-Campo R, Abelenda M, Paz Nava M, Puerta ML. Effect of cold acclimation on GSH, antioxidant enzymes and lipid peroxidation in brown adipose tissue. Biochemical journal. 1991 Jul 1;277(1):289-92.‌ Doi:10.1042/bj2770289.
62- Teramoto S, Uejima Y, Kitahara S, Ito H, Ouchi Y. Effect of whole body cold stress on glutathione metabolism in young and old mice. Journal of clinical biochemistry and nutrition. 1998;24(2):69-77.  Doi:10.3164/jcbn.24.69.
 

Files

Share

How to cite

Statistics