Ischemic preconditioning and exercise performance: A systematic review and meta-analysis

International Journal of Sports Physiology and Performance

Volumn 11, Issue 1, 2016, Pages 4-14

  Salvador, Amadeo F ^a   De Aguiar, Rafael A ^a   Lisbôa, Felipe D ^a   Pereira, Kayo L ^a   De Cruz, Rogério S O ^a   Caputo, Fabrizio ^a  

^a SANTA CATARINA STATE UNIVERSITY   (Brazil)

Author keywords

Aerobic; Anaerobic; Ergogenic aid; Muscle fatigue; Power; Sprint

Indexed keywords

AEROBIC EXERCISE; ANAEROBIC EXERCISE; CONFIDENCE INTERVAL; EFFECT SIZE; EXERCISE; HUMAN; ISCHEMIC PRECONDITIONING; SYSTEMATIC REVIEW; ATHLETIC PERFORMANCE; EXERCISE TEST; FITNESS; META ANALYSIS; PHYSICAL EDUCATION; PHYSIOLOGY; PROCEDURES;

ATHLETIC PERFORMANCE; EXERCISE TEST; HUMANS; ISCHEMIC PRECONDITIONING; PHYSICAL EDUCATION AND TRAINING; PHYSICAL FITNESS;

EID: 84957974844     PISSN: 15550265     EISSN: None     Source Type: Journal    
DOI: 10.1123/ijspp.2015-0204     Document Type: Article

References (87)

1. Carr AJ, Hopkins WG, Gore CJ. Effects of acute alkalosis and acidosis on performance: a meta-analysis. Sports Med. 2011;41(10):801-814. PubMed doi:10.2165/11591440-000000000-00000
2. Doherty M, Smith PM. Effects of caffeine ingestion on exercise testing: a meta-analysis. Int J Sport Nutr Exerc Metab. 2004;14(6):626-646. PubMed
3. Kilduff LP, Finn CV, Baker JS, Cook CJ, West DJ. Preconditioning strategies to enhance physical performance on the day of competition. Int J Sports Physiol Perform. 2013;8(6):677-681. PubMed
4. de Groot PC, Thijssen DH, Sanchez M, Ellenkamp R, Hopman MT. Ischemic preconditioning improves maximal performance in humans. Eur J Appl Physiol. 2010;108(1):141-146. PubMed doi:10.1007/s00421-009-1195-2
5. Przyklenk K, Bauer B, Ovize M, Kloner RA, Whittaker P. Regional ischemic 'preconditioning' protects remote virgin myocardium from subsequent sustained coronary occlusion. Circulation. 1993;87(3):893-899. PubMed doi:10.1161/01.CIR.87.3.893
6. Pang CY, Yang RZ, Zhong A, Xu N, Boyd B, Forrest CR. Acute isch-aemic preconditioning protects against skeletal muscle infarction in the pig. Cardiovasc Res. 1995;29(6):782-788. PubMed doi:10.1016/0008-6363(96)88613-5
7. Kida M, Fujiwara H, Ishida M, et al. Ischemic preconditioning preserves creatine phosphate and intracellular pH. Circulation. 1991;84(6):2495-2503. PubMed doi:10.1161/01.CIR.84.6.2495
8. Lawson CS, Downey JM. Preconditioning: state of the art myo-cardial protection. Cardiovasc Res. 1993;27(4):542-550. PubMed doi:10.1093/cvr/27.4.542
9. Andreas M, Schmid AI, Keilani M, et al. Effect of ischemic preconditioning in skeletal muscle measured by functional magnetic resonance imaging and spectroscopy: a randomized crossover trial. J Cardiovasc Magn Reson. 2011;13:32. PubMed doi:10.1186/1532-429X-13-32
10. Hausenloy DJ, Yellon DM. Remote ischaemic preconditioning: underlying mechanisms and clinical application. Cardiovasc Res. 2008;79(3):377-386. PubMed doi:10.1093/cvr/cvn114
11. Kido K, Suga T, Tanaka D, et al. Ischemic preconditioning accelerates muscle deoxygenation dynamics and enhances exercise endurance during the work-to-work test. Physiol Rep. 2015;3(5). PubMed doi:10.14814/phy2.12395
12. Foster GP, Giri PC, Rogers DM, Larson SR, Anholm JD. Ischemic preconditioning improves oxygen saturation and attenuates hypoxic pulmonary vasoconstriction at high altitude. High Alt Med Biol. 2014;15(2):155-161. PubMed doi:10.1089/ham.2013.1137
13. Barbosa TC, Machado AC, Braz ID, et al. Remote ischemic preconditioning delays fatigue development during handgrip exercise. Scand J Med Sci Sports. 2015;25(3):356-364. PubMed
14. Beaven CM, Cook CJ, Kilduff L, Drawer S, Gill N. Intermittent lower-limb occlusion enhances recovery after strenuous exercise. Appl Physiol Nutr Metab. 2012;37(6):1132-1139.
15. Crisafulli A, Tangianu F, Tocco F, et al. Ischemic preconditioning of the muscle improves maximal exercise performance but not maximal oxygen uptake in humans. J Appl Physiol. 2011;111(2):530-536.
16. Jean-St-Michel E, Manlhiot C, Li J, et al. Remote preconditioning improves maximal performance in highly trained athletes. Med Sci Sports Exerc. 2011;43(7):1280-1286. PubMed doi:10.1249/MSS.0b013e318206845d
17. Lalonde F, Curnier D. Can anaerobic performance be improved by remote ischemic preconditioning? J Strength Cond Res. 2015;29(1):80-85. PubMed
18. Hittinger EA, Maher JL, Nash MS, et al. Ischemic preconditioning does not improve peak exercise capacity at sea level or simulated high altitude in trained male cyclists. Appl Physiol Nutr Metab. 2015;40(1):65-71. PubMed
19. Bailey TG, Jones H, Gregson W, Atkinson G, Cable NT, Thijssen DH. Effect of ischemic preconditioning on lactate accumulation and running performance. Med Sci Sports Exerc. 2012;44(11):2084-2089. PubMed doi:10.1249/MSS.0b013e318262cb17
20. Kjeld T, Rasmussen MR, Jattu T, Nielsen HB, Secher NH. Ischemic preconditioning of one forearm enhances static and dynamic apnea. Med Sci Sports Exerc. 2014;46(1):151-155. PubMed doi:10.1249/MSS.0b013e3182a4090a
21. Kraus AS, Pasha EP, Machin DR, Alkatan M, Kloner RA, Tanaka H. Bilateral upper limb remote ischemic preconditioning improves anaerobic power. Open Sports Med J. 2015;9:1-6. doi:10.2174/1874387001509010001
22. Paixão RC, da Mota GR, Marocolo M. Acute effect of isch-emic preconditioning is detrimental to anaerobic performance in cyclists. Int J Sports Med. 2014;35(11):912-915. PubMed doi:10.1055/s-0034-1372628
23. Foster G P, Westerdahl DE, Foster LA, Hsu J V, Anholm JD. Isch-emic preconditioning of the lower extremity attenuates the normal hypoxic increase in pulmonary artery systolic pressure. Respir Physiol Neurobiol. 2011;179(2-3):248-253. PubMed doi:10.1016/j. resp.2011.09.001
24. Gibson N, White J, Neish M, Murray A. Effect of ischemic preconditioning on land-based sprinting in team-sport athletes. Int J Sports Physiol Perform. 2013;8(6):671-676. PubMed
25. Tocco F, Marongiu E, Ghiani G, et al. Muscle ischemic preconditioning does not improve performance during self-paced exercise. Int J Sports Med. 2015;36(1):9-15. PubMed
26. Clevidence MW, Mowery RE, Kushnick MR. The effects of isch-emic preconditioning on aerobic and anaerobic variables associated with submaximal cycling performance. Eur J Appl Physiol. 2012;112(10):3649-3654. PubMed doi:10.1007/s00421-012-2345-5
27. Borenstein M. Meta-Analysis: Computing Treatment Effects and Effect Sizes. West Sussex, UK: Wiley; 2009.
28. Hedges LV, Olkin I. Statistical Methods for Meta-Analysis. London, UK: Academic Press; 1985.
29. Rothstein HR, Sutton AJ, Borenstein M, eds. Publication Bias in Meta-Analysis. West Sussex, UK: Wiley; 2005. doi:10.1002/0470870168
30. Borenstein M, Hedges L, Higgins J, Rothstein H. Introduction to Meta-Analysis. West Sussex, UK: Wiley; 2009. doi:10.1002/9780470743386
31. Gastin PB. Energy system interaction and relative contribution during maximal exercise. Sports Med. 2001;31(10):725-741. PubMed doi:10.2165/00007256-200131100-00003
32. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74(5):1124-1136. PubMed doi:10.1161/01.CIR.74.5.1124
33. Hopkins WG. A spreadsheet for combining outcomes from several subject groups. Sportscience. 2006;10:51-53 sportsci.org/2006/wghcom.htm.
34. Hopkins WG. A spreadsheet for deriving a confdence interval, mechanistic inference and clinical inference from a P value. Sportscience. 2007;11:16-20. http://www.sportsci.org/2007/wghinf.htm
35. Hopkins WG. Probabilities of clinical or practical signifcance. Sport-science. 2002;6. http://www.sportsci.org/jour/0201/wghprob.htm
36. Hopkins WG, Marshall SW, Batterham AM, Hanin J. Progressive statistics for studies in sports medicine and exercise science. Med Sci Sports Exerc. 2009;41(1):3-13. PubMed doi:10.1249/MSS.0b013e31818cb278
37. Gibson N, Mahony B, Tracey C, Fawkner S, Murray A. Effect of ischemic preconditioning on repeated sprint ability in team sport athletes. J Sports Sci. 2015;33(11):1182-1188. PubMed
38. AT P-channel dependent mechanism. Circulation. 2007;116(12):1386-1395. PubMed doi:10.1161/Circu-lationAHA.106.653782
39. Xie JJ, Liao XL, Chen WG, et al. Remote ischaemic preconditioning reduces myocardial injury in patients undergoing heart valve surgery: randomised controlled trial. Heart. 2012;98(5):384-388. PubMed doi:10.1136/heartjnl-2011-300860
40. Wu ZK, Tarkka MR, Pehkonen E, Kaukinen L, Honkonen EL, Kaukinen S. Beneficial effects of ischemic preconditioning on right ventricular function after coronary artery bypass grafting. Ann Thorac Surg. 2000;70(5):1551-1557. PubMed doi:10.1016/S0003-4975(00)01850-6
41. Wu ZK, Tarkka MR, Pehkonen E, Kaukinen L, Honkonen EL, Kaukinen S. Ischaemic preconditioning has a benefcial effect on left ventricular haemodynamic function after a coronary artery biopass grafting operation. Scand Cardiovasc J. 2000;34(3):247-253. PubMed
42. Hittinger EA, Maher JL, Nash MS, et al. Ischemic preconditioning does not improve peak exercise capacity at sea level or simulated high altitude in trained male cyclists. Appl Physiol Nutr Metab. 2015;40(1):65-71. PubMed doi:10.1139/apnm-2014-0080
43. Enko K, Nakamura K, Yunoki K, et al. Intermittent arm ischemia induces vasodilatation of the contralateral upper limb. J Physiol Sci. 2011;61(6):507-513. PubMed doi:10.1007/s12576-011-0172-9
44. Kraemer R, Lorenzen J, Kabbani M, et al. Acute effects of remote ischemic preconditioning on cutaneous microcirculation-a controlled prospective cohort study. BMC Surg. 2011;11:32. PubMed doi:10.1186/1471-2482-11-32
45. Bailey TG, Birk GK, Cable NT, et al. Remote ischemic preconditioning prevents reduction in brachial artery fow-mediated dilation after strenuous exercise. Am J Physiol Heart Circ Physiol. 2012;303(5):H533-H538. PubMed doi:10.1152/ajpheart.00272.2012
46. Horiuchi M, Endo J, Thijssen DH. Impact of ischemic preconditioning on functional sympatholysis during handgrip exercise in humans. Physiol Rep. 2015;3(2). PubMed doi:10.14814/phy2.12304
47. Vander Heide RS, Reimer KA, Jennings RB. Adenosine slows ischae mic metabolism in canine myocardium in vitro: relationship to ischaemic preconditioning. Cardiovasc Res. 1993;27(4):669-673. PubMed doi:10.1093/cvr/27.4.669
48. Maldonado C, Pushpakumar SB, Perez-Abadia G, Arumugam S, Lane AN. Administration of exogenous adenosine triphosphate to ischemic skeletal muscle induces an energy-sparing effect: role of adenosine receptors. J Surg Res. 2013;181(1):e15-e22. PubMed doi:10.1016/j. jss.2012.06.033
49. + currents during metabolic inhibition in guinea pig ventricular myocytes. Can J Physiol Pharmacol. 2011;89(3):187-196. PubMed doi:10.1139/Y11-010
50. AT P channel. Am J Physiol. 1994;266(2 Pt 2):H829-H839. PubMed
51. Amann M, Runnels S, Morgan DE, et al. On the contribution of group III and IV muscle afferents to the circulatory response to rhythmic exercise in humans. J Physiol. 2011;589(Pt 15):3855-3866. PubMed doi:10.1113/jphysiol.2011.209353
52. Swyers T, Redford D, Larson DF. Volatile anesthetic-induced preconditioning. Perfusion. 2014;29(1):10-15. PubMed doi:10.1177/0267659113503975
53. Dragasis S, Bassiakou E, Iacovidou N, et al. The role of opioid receptor agonists in ischemic preconditioning. Eur J Pharmacol. 2013;720(1-3):401-408. PubMed doi:10.1016/j.ejphar.2013.10.001
54. Leal AK, Yamauchi K, Kim J, Ruiz-Velasco V, Kaufman MP. Peripheral delta-opioid receptors attenuate the exercise pressor refex. Am J Physiol Heart Circ Physiol. 2013;305(8):H1246-H1255. PubMed doi:10.1152/ajpheart.00116.2013
55. Amann M, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA. Opioid-mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans. J Physiol. 2009;587(Pt 1):271-283. PubMed doi:10.1113/jphysiol.2008.163303
56. Kaufman MP, Hayes SG. The exercise pressor refex. Clin Autonom Res. 2002;12(6):429-439. doi:10.1007/s10286-002-0059-1
57. Meintjes AF, Nobrega AC, Fuchs IE, Ally A, Wilson LB. Attenuation of the exercise pressor refex: effect of opioid agonist on substance P release in L-7 dorsal horn of cats. Circ Res. 1995;77(2):326-334. PubMed doi:10.1161/01.RES.77.2.326
58. AT P channel. Annu Rev Physiol. 2000;62:79-109. PubMed doi:10.1146/annurev.physiol.62.1.79
59. Downey JM, Davis AM, Cohen MV. Signaling pathways in ischemic preconditioning. Heart Fail Rev. 2007;12(3-4):181-188. PubMed doi:10.1007/s10741-007-9025-2
60. Finsterer J. Biomarkers of peripheral muscle fatigue during exercise. BMC Musculoskelet Disord. 2012;13:218. PubMed doi:10.1186/1471-2474-13-218
61. Radak Z, Zhao Z, Koltai E, Ohno H, Atalay M. Oxygen consumption and usage during physical exercise: the balance between oxidative stress and ROS-dependent adaptive signaling. Antioxid Redox Signal. 2013;18(10):1208-1246. PubMed doi:10.1089/ars.2011.4498
62. Sharma V, Cunniffe B, Verma AP, Cardinale M, Yellon D. Characterization of acute ischemia-related physiological responses associated with remote ischemic preconditioning: a randomized controlled, crossover human study. Physiol Rep. 2014;2(11). PubMed doi:10.14814/phy2.12200
63. Cormie P, McGuigan MR, Newton RU. Developing maximal neuro-muscular power: part 1-biological basis of maximal power production. Sports Med. 2011;41(1):17-38. PubMed doi:10.2165/11537690-000000000-00000
64. Phillips DJ, Petrie SG, Zhou BH, Guanche CA, Baratta RV. Myoelec-tric and mechanical changes elicited by ischemic preconditioning in the feline hindlimb. J Electromyogr Kinesiol. 1997;7(3):187-192.
65. Loukogeorgakis SP, Panagiotidou AT, Broadhead MW, Donald A, Deanfeld JE, Mac Allister RJ. Remote ischemic preconditioning provides early and late protection against endothelial ischemia-reperfusion injury in humans: role of the autonomic nervous system. J Am Coll Cardiol. 2005;46(3):450-456. PubMed doi:10.1016/j. jacc.2005.04.044
66. Marber MS, Latchman DS, Walker JM, Yellon DM. Cardiac stress protein elevation 24 hours after brief ischemia or heat stress is associated with resistance to myocardial infarction. Circulation. 1993;88(3):1264-1272. PubMed doi:10.1161/01.CIR.88.3.1264
67. Shinmura K, Nagai M, Tamaki K, Tani M, Bolli R. COX-2-derived prostacyclin mediates opioid-induced late phase of preconditioning in isolated rat hearts. Am J Physiol Heart Circ Physiol. 2002;283(6):H2534-H2543. PubMed doi:10.1152/ajp-heart.00209.2002
68. Hausenloy DJ, Yellon DM. The second window of preconditioning (SWOP): where are we now? Cardiovasc Drugs Ther. 2010;24(3):235-254.
69. Randhawa PK, Bali A, Singh Jaggi AS. RIPC for multiorgan salvage in clinical settings: evolution of concept, evidences and mechanisms. Eur J Pharmacol. 2015 5;746:317-332. PubMed
70. Jones H, Hopkins N, Bailey TG, Green DJ, Cable NT, Thijssen DH. Seven-day remote ischemic preconditioning improves local and systemic endothelial function and microcirculation in healthy humans. Am J Hypertens. 2014;27(7):918-925. PubMed doi:10.1093/ajh/hpu004
71. Jones H, Nyakayiru J, Bailey TG, et al. Impact of eight weeks of repeated ischaemic preconditioning on brachial artery and cutaneous microcirculatory function in healthy males. Eur J Prev Cardiol. 2015;22(8):1083-1087. PubMed
72. Depre C, Park JY, Shen YT, et al. Molecular mechanisms mediating preconditioning following chronic ischemia differ from those in classical second window. Am J Physiol Heart Circ Physiol. 2010;299(3):H752-H762. PubMed doi:10.1152/ajpheart.00147.2010
73. Shen YT, Depre C, Yan L, et al. Repetitive ischemia by coronary stenosis induces a novel window of ischemic preconditioning. Circulation. 2008;118(19):1961-1969. PubMed doi:10.1161/CIRCU-LATIONAHA.108.788240
74. Patterson SD, Bezodis NE, Glaister M, Pattison JR. The effect of ischemic preconditioning on repeated sprint cycling performance. Med Sci Sports Exerc. 2015;47(8):1652-1658. PubMed
75. Bogdanis GC, Nevill ME, Boobis LH, Lakomy HK. Contribution of phosphocreatine and aerobic metabolism to energy supply during repeated sprint exercise. J Appl Physiol. 1996;80(3):876-884. PubMed
76. Alkhulaif AM, Pugsley WB, Yellon DM. The Influence of the time period between preconditioning ischemia and prolonged ischemia on myocardial protection. Cardioscience. 1993;4(3):163-169. PubMed
77. Kavazis AN. Exercise preconditioning of the myocardium. Sports Med. 2009;39(11):923-935. PubMed doi:10.2165/11317870-000000000-00000
78. Marongiu E, Crisafulli A. Cardioprotection acquired through exercise: the role of ischemic preconditioning. Curr Cardiol Rev. 2014;10(4):336-348. PubMed doi:10.2174/1573403X10666140404110229
79. Hopkins WG, Hawley JA, Burke LM. Design and analysis of research on sport performance enhancement. Med Sci Sports Exerc. 1999;31(3):472-485. PubMed doi:10.1097/00005768-199903000-00018
80. Haji Mohd Yasin NA, Herbison P, Saxena P, Praporski S, Konstantinov IE. The role of remote ischemic preconditioning in organ protection after cardiac surgery: a meta-analysis. J Surg Res. 2014;186(1):207-216. PubMed doi:10.1016/j.jss.2013.09.006
81. Bushell AJ, Klenerman L, Davies H, Grierson I, McArdle A, Jackson MJ. Ischaemic preconditioning of skeletal muscle 2: investigation of the potential mechanisms involved. J Bone Joint Surg Br. 2002;84(8):1189-1193. PubMed doi:10.1302/0301-620X.84B8.9362
82. Bushell AJ, Klenerman L, Taylor S, et al. Ischaemic preconditioning of skeletal muscle 1: protection against the structural changes induced by ischaemia/reperfusion injury. J Bone Joint Surg Br. 2002;84(8):1184-1188. PubMed doi:10.1302/0301-620X.84B8.9361
83. Shaw JA, Murray DG. The relationship between tourniquet pressure and underlying soft-tissue pressure in the thigh. J Bone Joint Surg Am. 1982;64(8):1148-1152. PubMed
84. Loenneke JP, Fahs CA, Rossow LM, et al. Effects of cuff width on arterial occlusion: implications for blood fow restricted exercise. Eur J Appl Physiol. 2012;112(8):2903-2912. PubMed doi:10.1007/s00421-011-2266-8
85. Dempsey JA, Wagner PD. Exercise-induced arterial hypoxemia. J Appl Physiol. 1999;87(6):1997-2006. PubMed
86. Iida H, Kurano M, Takano H, et al. Hemodynamic and neurohumoral responses to the restriction of femoral blood fow by KAATSU in healthy subjects. Eur J Appl Physiol. 2007;100(3):275-285. PubMed doi:10.1007/s00421-007-0430-y
87. Tucker R. The anticipatory regulation of performance: the physiological basis for pacing strategies and the development of a perception-based model for exercise performance. Br J Sports Med. 2009;43(6):392-400. PubMed doi:10.1136/bjsm.2008.050799