EXERCISE-INDUCED CHANGES IN LIPID AND PROTEIN OXIDATION IN THE BLOOD OF MARES AND STALLIONS OF ENGLISH HALF-BREED HORSES LIVING IN THE POMERANIAN REGION (NORTHERN POLAND)
Keywords:
English half-breed horses, exercise, blood, 2-thiobarbituric acid reactive substances (TBARS), carbonyl groups of oxidatively modified proteins, total antioxidant capacity (TAC)
Abstract
Physical exertion and exercise-induced stress in horses vary according to the equestrian discipline and breed. The correct training programme aims to adapt the horse's organism to the physiological changes that occur during intense physical exertion. The aim of our research was to investigate the effect of physical training on the levels of markers of oxidative stress [2-thiobarbituric acid reactive substances (TBARS), carbonyl groups of oxidatively modified proteins, total antioxidant capacity (TAC)] in the peripheral blood of healthy English half-breed horses. Nine healthy English half-breed horses (7 mares and 8 stallions) living in the village of Karlikowo, in the administrative district of GminaKrokowa, within the Puck district, Pomeranian Voivodeship, in northern Poland were used in this study. Blood was collected from the animals' jugular veins in the morning, 90 min after feeding, while the horses were in the stable and immediately after exercise. The training started at 10:00 a.m., lasted 1 hour and consisted of a cross-country ride at a walk (5 mins), a trot (15 mins), a walk (10 mins), a trot (10 mins), a walk (5 mins), a canter (5 mins) and a walk (10 mins).The results of our study showed that blood levels of TBARS, as a biomarker of lipid peroxidation, showed a non-significant change in both mares and stallions immediately after exercise compared to the resting period. Blood levels of aldehydic and ketonic derivatives of oxidatively modified proteins were reduced in both mares and stallions after exercise compared to pre-exercise levels. These reductions were statistically significant. In the blood of mares and stallions, TAC levels were increased after exercise compared to pre-exercise levels. This increase was not statistically significant. The results of our study showed that exercise did not induce oxidative stress in the blood of English half-breeds mares and stallions. These results would provide valuable information for understanding the adaptation of horses to exercise.
References
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28. Lamprecht M, Greilberger J, Oettl K. Analytical aspects of oxidatively modified substances in sports and exercises. Nutrition. 2004;20(7-8):728-730. doi:10.1016/j.nut.2004.04.016.
29. Leeuwenburgh C, Heinecke JW. Oxidative stress and antioxidants in exercise. Curr Med Chem. 2001;8(7):829-838. doi:10.2174/0929867013372896.
30. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 1990;186:464-478. doi:10.1016/0076-6879(90)86141-h.
31. Levine RL, Stadtman ER. Oxidative modification of proteins during aging. ExpGerontol. 2001;36(9):1495-1502. doi:10.1016/s0531-5565(01)00135-8.
32. Lindner A, Signorini R, Brero L, Arn E, Mancini R, Enrique A. Effect of conditioning horses with short intervals at high speed on biochemical variables in blood. Equine Vet J Suppl. 2006;(36):88-92. doi:10.1111/j.2042-3306.2006.tb05519.x.
33. Lindner A, Wäschle S, Sasse HH. Physiological and blood biochemical variables in horses exercising on a treadmill submerged in water. J Anim Physiol Anim Nutr (Berl). 2012;96(4):563-569. doi:10.1111/j.1439-0396.2011.01179.x.
34. Luna D, Vásquez RA, Rojas M, Tadich TA. Welfare Status of Working Horses and Owners' Perceptions of Their Animals. Animals (Basel). 2017;7(8):56. doi:10.3390/ani7080056.
35. Machlin LJ, Bendich A. Free radical tissue damage: protective role of antioxidant nutrients. FASEB J. 1987;1(6):441-445.
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37. Marin DP, Bolin AP, Campoio TR, Guerra BA, Otton R. Oxidative stress and antioxidant status response of handball athletes: implications for sport training monitoring. IntImmunopharmacol. 2013;17(2):462-470. doi:10.1016/j.intimp.2013.07.009.
38. Nagy A, Dyson SJ, Murray JK. A veterinary review of endurance riding as an international competitive sport. Vet J. 2012;194(3):288-293. doi:10.1016/j.tvjl.2012.06.022.
39. Naito Y, Takagi T, Handa O, Yoshikawa T. Lipid hydroperoxide-derived modification of proteins in gastrointestinal tract. SubcellBiochem. 2014;77:137-148. doi:10.1007/978-94-007-7920-4_12.
40. Niki E. Do antioxidants impair signaling by reactive oxygen species and lipid oxidation products?. FEBS Lett. 2012;586(21):3767-3770. doi:10.1016/j.febslet.2012.09.025.
41. Ott EC, Cavinder CA, Wang S, Smith T, Lemley CO, Dinh TTN. Oxidative stress biomarkers and free amino acid concentrations in the blood plasma of moderately exercised horses indicate adaptive response to prolonged exercise training. J Anim Sci. 2022;100(4):skac086. doi:10.1093/jas/skac086.
42. Packer L, Cadenas E, Davies KJ. Free radicals and exercise: an introduction. Free RadicBiol Med. 2008;44(2):123-125. doi:10.1016/j.freeradbiomed.2007.05.031.
43. Palmieri B, Sblendorio V. Oxidative stress detection: what for? Part II. Eur Rev Med Pharmacol Sci. 2007;11(1):27-54.
44. Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev. 2008;88(4):1243-1276. doi:10.1152/physrev.00031.2007.
45. Radak Z, Ishihara K, Tekus E, Varga C, Posa A, Balogh L, Boldogh I, Koltai E. Exercise, oxidants, and antioxidants change the shape of the bell-shaped hormesis curve. Redox Biol. 2017;12:285-290. doi:10.1016/j.redox.2017.02.015.
46. Reichmann D, Voth W, Jakob U. Maintaining a Healthy Proteome during Oxidative Stress. Mol Cell. 2018;69(2):203-213. doi:10.1016/j.molcel.2017.12.021.
47. Romero FJ, Bosch-Morell F, Romero MJ, et al. Lipid peroxidation products and antioxidants in human disease. Environ Health Perspect. 1998;106Suppl 5(Suppl 5):1229-1234. doi:10.1289/ehp.98106s51229.
48. Samardzic K, Rodgers KJ. Oxidised protein metabolism: recent insights. Biol Chem. 2017;398(11):1165-1175. doi:10.1515/hsz-2017-0124.
49. Shono S, Gin A, Minowa F, Okubo K, Mochizuki M. The Oxidative Stress Markers of Horses-the Comparison with Other Animals and the Influence of Exercise and Disease. Animals (Basel). 2020;10(4):617. doi:10.3390/ani10040617.
50. Toyama BH, Hetzer MW. Protein homeostasis: live long, won't prosper. Nat Rev Mol Cell Biol. 2013;14(1):55-61. doi:10.1038/nrm3496.
51. Tsubone H, Hanafusa M, Endo M, Manabe N, Hiraga A, Ohmura H, Aida H. Effect of Treadmill Exercise and Hydrogen-rich Water Intake on Serum Oxidative and Anti-oxidative Metabolites in Serum of Thoroughbred Horses. J Equine Sci. 2013;24(1):1-8. doi:10.1294/jes.24.1.
52. vanWeeren PR, Back W. Technological advances in equestrian sports: are they beneficial for both performance and welfare?. Vet J. 2014;199(3):313-314. doi:10.1016/j.tvjl.2013.12.009.
53. Viña J, Gomez-Cabrera MC, Lloret A, Marquez R, Miñana JB, Pallardó FV, Sastre J. Free radicals in exhaustive physical exercise: mechanism of production, and protection by antioxidants. IUBMB Life. 2000;50(4-5):271-277. doi:10.1080/713803729.
54. Williams CA. The effect of oxidative stress during exercise in the horse. J Anim Sci. 2016;94(10):4067-4075. doi:10.2527/jas.2015-9988.
55. Zar J.H. Biostatistical Analysis. 4th ed., Prentice-Hall Inc., Englewood Cliffs, New Jersey, 1999.
2. Atock MA, Williams RB. Welfare of competition horses. Rev Sci Tech. 1994;13(1):217-232. doi:10.20506/rst.13.1.765.
3. Ayala A, Muñoz MF, Argüelles S. Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev. 2014;2014:360438. doi:10.1155/2014/360438.
4. Barclay JK, Hansel M. Free radicals may contribute to oxidative skeletal muscle fatigue. Can J PhysiolPharmacol. 1991;69(2):279-284. doi:10.1139/y91-043.
5. Bentley DJ, Ackerman J, Clifford T, Slattery KS. Acute and Chronic Effects of Antioxidant Supplementation on Exercise Performance. In: Lamprecht M, ed. Antioxidants in Sport Nutrition. Boca Raton (FL): CRC Press/Taylor & Francis; 2015.
6. BrkljačaBottegaro N, Gotić J, Šuran J, Brozić D, Klobučar K, Bojanić K, Vrbanac Z. Effect of prolonged submaximal exercise on serum oxidative stress biomarkers (d-ROMs, MDA, BAP) and oxidative stress index in endurance horses. BMC Vet Res. 2018;14(1):216. doi:10.1186/s12917-018-1540-y.
7. Cadenas E, Davies KJ. Mitochondrial free radical generation, oxidative stress, and aging. Free RadicBiol Med. 2000;29(3-4):222-230. doi:10.1016/s0891-5849(00)00317-8.
8. Campbell ML. The role of veterinarians in equestrian sport: a comparative review of ethical issues surrounding human and equine sports medicine. Vet J. 2013;197(3):535-540. doi:10.1016/j.tvjl.2013.05.021.
9. Chiaradia E, Avellini L, Rueca F, Spaterna A, Porciello F, Antonioni MT, Gaiti A. Physical exercise, oxidative stress and muscle damage in racehorses. Comp BiochemPhysiol B BiochemMol Biol. 1998;119(4):833-836. doi:10.1016/s0305-0491(98)10001-9.
10. deVries WR, Bernards NT, de Rooij MH, Koppeschaar HP. Dynamic exercise discloses different time-related responses in stress hormones. Psychosom Med. 2000;62(6):866-872. doi:10.1097/00006842-200011000-00017.
11. Demasi M, Augusto O, Bechara EJH, Bicev RN, Cerqueira FM, da Cunha FM, Denicola A, Gomes F, Miyamoto S, Netto LES, Randall LM, Stevani CV, Thomson L. Oxidative Modification of Proteins: From Damage to Catalysis, Signaling, and Beyond. Antioxid Redox Signal. 2021;35(12):1016-1080. doi:10.1089/ars.2020.8176.
12. Dubinina EE, Burmistrov SO, Khodov DA, Porotov IG. Okislitel'naiamodifikatsiiabelkovsyvorotkikrovicheloveka, metodeeopredeleniia [Oxidative modification of human serum proteins. A method of determining it]. Vopr Med Khim. 1995;41(1):24-26.
13. Escribano BM, Agüera EI, Rubio MD, Santisteban R, Vivo R, Agüera S, Tovar P. Utility of the discriminant analysis to categorize untrained Spanish Pure Bred horses on the basis of biochemical and muscle variables before and after a standardized exercise test. Res Vet Sci. 2011;91(3):e144-e148. doi:10.1016/j.rvsc.2011.03.006.
14. Ferlazzo A, Cravana C, Fazio E, Medica P. The different hormonal system during exercise stress coping in horses. Vet World. 2020;13(5):847-859. doi:10.14202/vetworld.2020.847-859.
15. Fisher-Wellman K, Bloomer RJ. Acute exercise and oxidative stress: a 30 year history. Dyn Med. 2009;8:1. Published 2009 Jan 13. doi:10.1186/1476-5918-8-1
16. Fomina NV, Fomina MA, Kalinin RE, Suchkov IA. [Oxidative carbonylation of vascular wall proteins in dynamics of experimental venous thrombosis]. AngiolSosudKhir. 2015;21(1):29-34.
17. Furtado T, Preshaw L, Hockenhull J, Wathan J, Douglas J, Horseman S, Smith R, Pollard D, Pinchbeck G, Rogers J, Hall C. How Happy Are Equine Athletes? Stakeholder Perceptions of Equine Welfare Issues Associated with Equestrian Sport. Animals (Basel). 2021;11(11):3228. doi:10.3390/ani11113228.
18. Gad AS, Khadrawy YA, El-Nekeety AA, Mohamed SR, Hassan NS, Abdel-Wahhab MA. Antioxidant activity and hepatoprotective effects of whey protein and Spirulina in rats. Nutrition. 2011;27(5):582-589. doi:10.1016/j.nut.2010.04.002.
19. Galaktionova LP, Molchanov AV, El'chaninova SA, VarshavskiĭBIa. Sostoianieperekisnogookisleniia u bol'nykh s iazvennoĭbolezn'iuzheludka i dvenadtsatiperstnoĭkishki [Lipid peroxidation in patients with gastric and duodenal peptic ulcers]. Klin Lab Diagn. 1998;(6):10-14.
20. Garcia YJ, Rodríguez-Malaver AJ, Peñaloza N. Lipid peroxidation measurement by thiobarbituric acid assay in rat cerebellar slices. J Neurosci Methods. 2005;144(1):127-135. doi:10.1016/j.jneumeth.2004.10.018.
21. Gross M, Baum O. Supplemental Antioxidants and Adaptation to Physical Training. In: Lamprecht M, ed. Antioxidants in Sport Nutrition. Boca Raton (FL): CRC Press/Taylor & Francis; 2015.
22. Holmes TQ, Brown AF. Champing at the Bit for Improvements: A Review of Equine Welfare in Equestrian Sports in the United Kingdom. Animals (Basel). 2022;12(9):1186. doi:10.3390/ani12091186.
23. Ji LL, Leichtweis S. Exercise and oxidative stress: Sources of free radicals and their impact on antioxidant systems. Age (Omaha). 1997;20(2):91-106. doi:10.1007/s11357-997-0009-x.
24. Kamyshnikov VS. A reference work for clinical and biochemical research and laboratory diagnostics. MEDpress-inform, Moscow, 2004.
25. Keener MM, Tumlin KI. The Triple-E Model: Advancing Equestrian Research with Perspectives from One Health. Animals (Basel). 2023;13(16):2642. doi:10.3390/ani13162642.
26. Kinnunen S, Hyyppä S, Lappalainen J, Oksala N, Venojärvi M, Nakao C, Hänninen O, Sen CK, Atalay M. Exercise-induced oxidative stress and muscle stress protein responses in trotters. Eur J Appl Physiol. 2005;93(4):496-501. doi:10.1007/s00421-004-1162-x.
27. Kirschvink N, de Moffarts B, Lekeux P. The oxidant/antioxidant equilibrium in horses. Vet J. 2008;177(2):178-191. doi:10.1016/j.tvjl.2007.07.033.
28. Lamprecht M, Greilberger J, Oettl K. Analytical aspects of oxidatively modified substances in sports and exercises. Nutrition. 2004;20(7-8):728-730. doi:10.1016/j.nut.2004.04.016.
29. Leeuwenburgh C, Heinecke JW. Oxidative stress and antioxidants in exercise. Curr Med Chem. 2001;8(7):829-838. doi:10.2174/0929867013372896.
30. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 1990;186:464-478. doi:10.1016/0076-6879(90)86141-h.
31. Levine RL, Stadtman ER. Oxidative modification of proteins during aging. ExpGerontol. 2001;36(9):1495-1502. doi:10.1016/s0531-5565(01)00135-8.
32. Lindner A, Signorini R, Brero L, Arn E, Mancini R, Enrique A. Effect of conditioning horses with short intervals at high speed on biochemical variables in blood. Equine Vet J Suppl. 2006;(36):88-92. doi:10.1111/j.2042-3306.2006.tb05519.x.
33. Lindner A, Wäschle S, Sasse HH. Physiological and blood biochemical variables in horses exercising on a treadmill submerged in water. J Anim Physiol Anim Nutr (Berl). 2012;96(4):563-569. doi:10.1111/j.1439-0396.2011.01179.x.
34. Luna D, Vásquez RA, Rojas M, Tadich TA. Welfare Status of Working Horses and Owners' Perceptions of Their Animals. Animals (Basel). 2017;7(8):56. doi:10.3390/ani7080056.
35. Machlin LJ, Bendich A. Free radical tissue damage: protective role of antioxidant nutrients. FASEB J. 1987;1(6):441-445.
36. MacNicol JL, Lindinger MI, Pearson W. A time-course evaluation of inflammatory and oxidative markers following high-intensity exercise in horses: a pilot study. J ApplPhysiol (1985). 2018;124(4):860-865. doi:10.1152/japplphysiol.00461.2017.
37. Marin DP, Bolin AP, Campoio TR, Guerra BA, Otton R. Oxidative stress and antioxidant status response of handball athletes: implications for sport training monitoring. IntImmunopharmacol. 2013;17(2):462-470. doi:10.1016/j.intimp.2013.07.009.
38. Nagy A, Dyson SJ, Murray JK. A veterinary review of endurance riding as an international competitive sport. Vet J. 2012;194(3):288-293. doi:10.1016/j.tvjl.2012.06.022.
39. Naito Y, Takagi T, Handa O, Yoshikawa T. Lipid hydroperoxide-derived modification of proteins in gastrointestinal tract. SubcellBiochem. 2014;77:137-148. doi:10.1007/978-94-007-7920-4_12.
40. Niki E. Do antioxidants impair signaling by reactive oxygen species and lipid oxidation products?. FEBS Lett. 2012;586(21):3767-3770. doi:10.1016/j.febslet.2012.09.025.
41. Ott EC, Cavinder CA, Wang S, Smith T, Lemley CO, Dinh TTN. Oxidative stress biomarkers and free amino acid concentrations in the blood plasma of moderately exercised horses indicate adaptive response to prolonged exercise training. J Anim Sci. 2022;100(4):skac086. doi:10.1093/jas/skac086.
42. Packer L, Cadenas E, Davies KJ. Free radicals and exercise: an introduction. Free RadicBiol Med. 2008;44(2):123-125. doi:10.1016/j.freeradbiomed.2007.05.031.
43. Palmieri B, Sblendorio V. Oxidative stress detection: what for? Part II. Eur Rev Med Pharmacol Sci. 2007;11(1):27-54.
44. Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev. 2008;88(4):1243-1276. doi:10.1152/physrev.00031.2007.
45. Radak Z, Ishihara K, Tekus E, Varga C, Posa A, Balogh L, Boldogh I, Koltai E. Exercise, oxidants, and antioxidants change the shape of the bell-shaped hormesis curve. Redox Biol. 2017;12:285-290. doi:10.1016/j.redox.2017.02.015.
46. Reichmann D, Voth W, Jakob U. Maintaining a Healthy Proteome during Oxidative Stress. Mol Cell. 2018;69(2):203-213. doi:10.1016/j.molcel.2017.12.021.
47. Romero FJ, Bosch-Morell F, Romero MJ, et al. Lipid peroxidation products and antioxidants in human disease. Environ Health Perspect. 1998;106Suppl 5(Suppl 5):1229-1234. doi:10.1289/ehp.98106s51229.
48. Samardzic K, Rodgers KJ. Oxidised protein metabolism: recent insights. Biol Chem. 2017;398(11):1165-1175. doi:10.1515/hsz-2017-0124.
49. Shono S, Gin A, Minowa F, Okubo K, Mochizuki M. The Oxidative Stress Markers of Horses-the Comparison with Other Animals and the Influence of Exercise and Disease. Animals (Basel). 2020;10(4):617. doi:10.3390/ani10040617.
50. Toyama BH, Hetzer MW. Protein homeostasis: live long, won't prosper. Nat Rev Mol Cell Biol. 2013;14(1):55-61. doi:10.1038/nrm3496.
51. Tsubone H, Hanafusa M, Endo M, Manabe N, Hiraga A, Ohmura H, Aida H. Effect of Treadmill Exercise and Hydrogen-rich Water Intake on Serum Oxidative and Anti-oxidative Metabolites in Serum of Thoroughbred Horses. J Equine Sci. 2013;24(1):1-8. doi:10.1294/jes.24.1.
52. vanWeeren PR, Back W. Technological advances in equestrian sports: are they beneficial for both performance and welfare?. Vet J. 2014;199(3):313-314. doi:10.1016/j.tvjl.2013.12.009.
53. Viña J, Gomez-Cabrera MC, Lloret A, Marquez R, Miñana JB, Pallardó FV, Sastre J. Free radicals in exhaustive physical exercise: mechanism of production, and protection by antioxidants. IUBMB Life. 2000;50(4-5):271-277. doi:10.1080/713803729.
54. Williams CA. The effect of oxidative stress during exercise in the horse. J Anim Sci. 2016;94(10):4067-4075. doi:10.2527/jas.2015-9988.
55. Zar J.H. Biostatistical Analysis. 4th ed., Prentice-Hall Inc., Englewood Cliffs, New Jersey, 1999.