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Sports Medicine
Published in: Sports Medicine 4/2016

01-04-2016 | Systematic Review

The Effects of Ischemic Preconditioning on Human Exercise Performance

Authors: Anthony V. Incognito, Jamie F. Burr, Philip J. Millar

Published in: Sports Medicine | Issue 4/2016

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Abstract

Background

Ischemic preconditioning (IPC) is the exposure to brief periods of circulatory occlusion and reperfusion in order to protect local or systemic organs against subsequent bouts of ischemia. IPC has also been proposed as a novel intervention to improve exercise performance in healthy and diseased populations.

Objective

The purpose of this systematic review is to analyze the evidence for IPC improving exercise performance in healthy humans.

Methods

Data were obtained using a systematic computer-assisted search of four electronic databases (MEDLINE, PubMed, SPORTDiscus, CINAHL), from January 1985 to October 2015, and relevant reference lists.

Results

Twenty-one studies met the inclusion criteria. The collective data suggest that IPC is a safe intervention that may be capable of improving time-trial performance. Available individual data from included studies demonstrate that IPC improved time-trial performance in 67 % of participants, with comparable results in athletes and recreationally active populations. The effects of IPC on power output, oxygen consumption, rating of perceived exertion, blood lactate accumulation, and cardiorespiratory measures are unclear. The within-study heterogeneity may suggest the presence of IPC responders and non-responders, which in combination with small sample sizes, likely confound interpretation of mean group data in the literature.

Conclusion

The ability of IPC to improve time-trial performance is promising, but the potential mechanisms responsible require further investigation. Future work should be directed toward identifying the individual phenotype and protocol that will best exploit IPC-mediated exercise performance improvements, facilitating its application in sport settings.
Literature
1.
Loukogeorgakis SP, Panagiotidou AT, Broadhead MW, et al. 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;46:450–6.CrossRefPubMed
2.
Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74:1124–36.CrossRefPubMed
3.
Shimizu M, Tropak M, Diaz RJ, et al. Transient limb ischaemia remotely preconditions through a humoral mechanism acting directly on the myocardium: evidence suggesting cross-species protection. Clin Sci (Lond). 2009;117:191–200.CrossRefPubMed
4.
Przyklenk K, Bauer B, Ovize M, et al. Regional ischemic ‘preconditioning’ protects remote virgin myocardium from subsequent sustained coronary occlusion. Circulation. 1993;87:893–9.CrossRefPubMed
5.
Botker HE, Kharbanda R, Schmidt MR, et al. Remote ischaemic conditioning before hospital admission, as a complement to angioplasty, and effect on myocardial salvage in patients with acute myocardial infarction: a randomised trial. Lancet. 2010;375:727–34.CrossRefPubMed
6.
Candilio L, Malik A, Ariti C, et al. Effect of remote ischaemic preconditioning on clinical outcomes in patients undergoing cardiac bypass surgery: a randomised controlled clinical trial. Heart. 2015;101:185–92.CrossRefPubMed
7.
Walsh SR, Tang TY, Kullar P, et al. Ischaemic preconditioning during cardiac surgery: systematic review and meta-analysis of perioperative outcomes in randomised clinical trials. Eur J Cardiothorac Surg. 2008;34:985–94.CrossRefPubMed
8.
Addison PD, Neligan PC, Ashrafpour H, et al. Noninvasive remote ischemic preconditioning for global protection of skeletal muscle against infarction. Am J Physiol Heart Circ Physiol. 2003;285:H1435–43.CrossRefPubMed
9.
Pang CY, Yang RZ, Zhong A, et al. Acute ischaemic preconditioning protects against skeletal muscle infarction in the pig. Cardiovasc Res. 1995;29:782–8.CrossRefPubMed
10.
Schroeder CA Jr, Lee HT, Shah PM, et al. Preconditioning with ischemia or adenosine protects skeletal muscle from ischemic tissue reperfusion injury. J Surg Res. 1996;63:29–34.CrossRefPubMed
11.
Lintz JA, Dalio MB, Joviliano EE, et al. Ischemic pre and postconditioning in skeletal muscle injury produced by ischemia and reperfusion in rats. Acta Cir Bras. 2013;28:441–6.CrossRefPubMed
12.
Enko K, Nakamura K, Yunoki K, et al. Intermittent arm ischemia induces vasodilatation of the contralateral upper limb. J Physiol Sci. 2011;61:507–13.CrossRefPubMed
13.
Horiuchi M, Endo J, Thijssen DH. Impact of ischemic preconditioning on functional sympatholysis during handgrip exercise in humans. Physiol Rep. 2015;3:e12304.CrossRefPubMedPubMedCentral
14.
Bailey TG, Birk GK, Cable NT, et al. Remote ischemic preconditioning prevents reduction in brachial artery flow-mediated dilation after strenuous exercise. Am J Physiol Heart Circ Physiol. 2012;303:H533–8.CrossRefPubMed
15.
Kharbanda RK, Mortensen UM, White PA, et al. Transient limb ischemia induces remote ischemic preconditioning in vivo. Circulation. 2002;106:2881–3.CrossRefPubMed
16.
Wang WZ, Stepheson LL, Fang XH, et al. Ischemic preconditioning-induced microvascular protection at a distance. J Reconstr Microsurg. 2004;20:175–81.CrossRefPubMed
17.
18.
Jean-St-Michel E, Manlhiot C, Li J, et al. Remote preconditioning improves maximal performance in highly trained athletes. Med Sci Sports Exerc. 2011;43:1280–6.CrossRefPubMed
19.
Bailey TG, Jones H, Gregson W, et al. Effect of ischemic preconditioning on lactate accumulation and running performance. Med Sci Sports Exerc. 2012;44:2084–9.CrossRefPubMed
20.
Kilduff LP, Finn CV, Baker JS, et al. Preconditioning strategies to enhance physical performance on the day of competition. Int J Sports Physiol Perform. 2013;8:677–81.PubMed
21.
Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol. 2009;62:e1–34.CrossRefPubMed
22.
Stewart LA, Clarke M, Rovers M, et al. Preferred Reporting Items for Systematic Review and Meta-Analyses of individual participant data: the PRISMA-IPD Statement. JAMA. 2015;313:1657–65.CrossRefPubMed
23.
Heusch G. Molecular basis of cardioprotection: signal transduction in ischemic pre-, post-, and remote conditioning. Circ Res. 2015;116:674–99.CrossRefPubMed
24.
Gastin PB. Energy system interaction and relative contribution during maximal exercise. Sports Med. 2001;31:725–41.CrossRefPubMed
25.
Clevidence MW, Mowery RE, Kushnick MR. The effects of ischemic preconditioning on aerobic and anaerobic variables associated with submaximal cycling performance. Eur J Appl Physiol. 2012;112:3649–54.CrossRefPubMed
26.
Cruz RS, De Aguiar RA, Turnes T, et al. Effects of ischemic preconditioning on maximal constant load cycling performance. J Appl Physiol (1985) 2015;119:961–7.
27.
Gibson N, White J, Neish M, et al. Effect of ischemic preconditioning on land-based sprinting in team-sport athletes. Int J Sports Physiol Perform. 2013;8:671–6.PubMed
28.
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:e12395.CrossRefPubMedPubMedCentral
29.
Tocco F, Marongiu E, Ghiani G, et al. Muscle ischemic preconditioning does not improve performance during self-paced exercise. Int J Sports Med. 2015;36:9–15.PubMed
30.
Marocolo M, da Mota GR, Pelegrini V, et al. Are the beneficial effects of ischemic preconditioning on performance partly a placebo effect? Int J Sports Med. 2015;36:822–5.CrossRefPubMed
31.
Kjeld T, Rasmussen MR, Jattu T, et al. Ischemic preconditioning of one forearm enhances static and dynamic apnea. Med Sci Sports Exerc. 2014;46:151–5.CrossRefPubMed
32.
Marocolo M, Willardson JM, Marocolo IC, et al. Ischemic preconditioning and placebo intervention improves resistance exercise performance. J Strength Cond Res. PMID: 26466134. doi:10.​1519/​JSC.​0000000000001232​.
33.
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. 1985;2011(111):530–6.
34.
Barbosa TC, Machado AC, Braz ID, et al. Remote ischemic preconditioning delays fatigue development during handgrip exercise. Scand J Med Sci Sports. 2015;25:356–64.CrossRefPubMed
35.
Foster GP, Westerdahl DE, Foster LA, et al. Ischemic preconditioning of the lower extremity attenuates the normal hypoxic increase in pulmonary artery systolic pressure. Respir Physiol Neurobiol. 2011;179:248–53.CrossRefPubMed
36.
Patterson SD, Bezodis NE, Glaister M, et al. The effect of ischemic preconditioning on repeated sprint cycling performance. Med Sci Sports Exerc. 2015;47:1652–8.CrossRefPubMed
37.
Gibson N, Mahony B, Tracey C, et al. Effect of ischemic preconditioning on repeated sprint ability in team sport athletes. J Sports Sci. 2015;33:1182–8.CrossRefPubMed
38.
Lalonde F, Curnier DY. Can anaerobic performance be improved by remote ischemic preconditioning? J Strength Cond Res. 2015;29:80–5.CrossRefPubMed
39.
Paixão RC, da Mota GR, Marocolo M. Acute effect of ischemic preconditioning is detrimental to anaerobic performance in cyclists. Int J Sports Med. 2014;35:912–5.CrossRefPubMed
40.
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;40:65–71.CrossRefPubMed
41.
El Messaoudi S, Vissers A, Thijssen D, et al. The effect of remote ischemic preconditioning on exercise-induced plasma troponin I appearance in healthy volunteers. Int J Cardiol. 2013;168:1612–3.CrossRefPubMed
42.
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;22:1083–7.CrossRefPubMed
43.
Patterson SD, Bezodis NE, Glaister M, et al. The effect of ischemic preconditioning on repeated sprint cycling performance. Med Sci Sports Exerc. 2014;47:1652–8.CrossRef
44.
Battipaglia I, Scalone G, Milo M, et al. Upper arm intermittent ischaemia reduces exercise-related increase of platelet reactivity in patients with obstructive coronary artery disease. Heart. 2011;97:1298–303.CrossRefPubMed
45.
46.
Bouchard C, Rankinen T. Individual differences in response to regular physical activity. Med Sci Sports Exerc. 2001;33:S446–51.
47.
Brevoord D, Kranke P, Kuijpers M, et al. Remote ischemic conditioning to protect against ischemia-reperfusion injury: a systematic review and meta-analysis. PLoS One. 2012;7:e42179.CrossRefPubMedPubMedCentral
48.
Lee TM, Su SF, Chou TF, et al. Loss of preconditioning by attenuated activation of myocardial ATP-sensitive potassium channels in elderly patients undergoing coronary angioplasty. Circulation. 2002;105:334–40.CrossRefPubMed
49.
Laskey WK, Beach D. Frequency and clinical significance of ischemic preconditioning during percutaneous coronary intervention. J Am Coll Cardiol. 2003;42:998–1003.CrossRefPubMed
50.
Sharma V, Cunniffe B, Verma AP, et al. Characterization of acute ischemia-related physiological responses associated with remote ischemic preconditioning: a randomized controlled, crossover human study. Physiol Rep. 2014;2:e12200.CrossRefPubMedPubMedCentral
51.
Loukogeorgakis SP, Williams R, Panagiotidou AT, et al. Transient limb ischemia induces remote preconditioning and remote postconditioning in humans by a K(ATP)-channel dependent mechanism. Circulation. 2007;116:1386–95.CrossRefPubMed
52.
Hausenloy DJ, Yellon DM. The second window of preconditioning (SWOP) where are we now? Cardiovasc Drugs Ther. 2010;24:235–54.CrossRefPubMed
53.
Lalonde F, Poirier P, Arvisais D, et al. Exercise-induced ischemic preconditioning and the potential application to cardiac rehabilitation: a systematic review. J Cardiopulm Rehabil Prev. 2015;35:93–102.CrossRefPubMed
54.
Niccoli G, Altamura L, Fabretti A, et al. Ethanol abolishes ischemic preconditioning in humans. J Am Coll Cardiol. 2008;51:271–5.CrossRefPubMed
55.
Riksen NP, Zhou Z, Oyen WJ, et al. Caffeine prevents protection in two human models of ischemic preconditioning. J Am Coll Cardiol. 2006;48:700–7.CrossRefPubMed
56.
Perera V, Gross AS, Xu H, et al. Pharmacokinetics of caffeine in plasma and saliva, and the influence of caffeine abstinence on CYP1A2 metrics. J Pharm Pharmacol. 2011;63:1161–8.CrossRefPubMed
57.
Jacobsen D, Sebastian CS, Dies DF, et al. Kinetic interactions between 4-methylpyrazole and ethanol in healthy humans. Alcohol Clin Exp Res. 1996;20:804–9.CrossRefPubMed
58.
59.
Liem DA, Verdouw PD, Ploeg H, et al. Sites of action of adenosine in interorgan preconditioning of the heart. Am J Physiol Heart Circ Physiol. 2002;283:H29–37.CrossRefPubMed
60.
Steensrud T, Li J, Dai X, et al. Pretreatment with the nitric oxide donor SNAP or nerve transection blocks humoral preconditioning by remote limb ischemia or intra-arterial adenosine. Am J Physiol Heart Circ Physiol. 2010;299:H1598–603.CrossRefPubMed
61.
Redington KL, Disenhouse T, Strantzas SC, et al. Remote cardioprotection by direct peripheral nerve stimulation and topical capsaicin is mediated by circulating humoral factors. Basic Res Cardiol. 2012;107:241.CrossRefPubMed
62.
Moses MA, Addison PD, Neligan PC, et al. Mitochondrial KATP channels in hindlimb remote ischemic preconditioning of skeletal muscle against infarction. Am J Physiol Heart Circ Physiol. 2005;288:H559–67.CrossRefPubMed
63.
Mansour Z, Bouitbir J, Charles AL, et al. Remote and local ischemic preconditioning equivalently protects rat skeletal muscle mitochondrial function during experimental aortic cross-clamping. J Vasc Surg. 2012;55(497–505):e1.PubMed
64.
Thaveau F, Zoll J, Rouyer O, et al. Ischemic preconditioning specifically restores complexes I and II activities of the mitochondrial respiratory chain in ischemic skeletal muscle. J Vasc Surg. 2007;46:541–7 (discussion 7).
65.
Costa F, Christensen NJ, Farley G, et al. NO modulates norepinephrine release in human skeletal muscle: implications for neural preconditioning. Am J Physiol Regul Integr Comp Physiol. 2001;280:R1494–8.PubMed
66.
Pudupakkam S, Harris KA, Jamieson WG, et al. Ischemic tolerance in skeletal muscle: role of nitric oxide. Am J Physiol. 1998;275:H94–9.PubMed
67.
Rassaf T, Totzeck M, Hendgen-Cotta UB, et al. Circulating nitrite contributes to cardioprotection by remote ischemic preconditioning. Circ Res. 2014;114:1601–10.CrossRefPubMed
68.
Larsen FJ, Schiffer TA, Borniquel S, et al. Dietary inorganic nitrate improves mitochondrial efficiency in humans. Cell Metab. 2011;13:149–59.CrossRefPubMed
69.
Seyfarth M, Richardt G, Mizsnyak A, et al. Transient ischemia reduces norepinephrine release during sustained ischemia. Neural preconditioning in isolated rat heart. Circ Res. 1996;78:573–80.CrossRefPubMed
70.
Kimura M, Ueda K, Goto C, et al. Repetition of ischemic preconditioning augments endothelium-dependent vasodilation in humans: role of endothelium-derived nitric oxide and endothelial progenitor cells. Arterioscler Thromb Vasc Biol. 2007;27:1403–10.CrossRefPubMed
71.
Saes GF, Zerati AE, Wolosker N, et al. Remote ischemic preconditioning in patients with intermittent claudication. Clinics (Sao Paulo). 2013;68:495–9.CrossRefPubMedPubMedCentral
72.
Delagarde H, Ouadraougo N, Grall S, et al. Remote ischaemic preconditioning in intermittent claudication. Arch Cardiovasc Dis. 2015;108:472–9.CrossRefPubMed
73.
Slagsvold KH, Rognmo O, Hoydal M, et al. Remote ischemic preconditioning preserves mitochondrial function and influences myocardial microRNA expression in atrial myocardium during coronary bypass surgery. Circ Res. 2014;114:851–9.CrossRefPubMed
74.
Slagsvold KH, Moreira JB, Rognmo O, et al. Remote ischemic preconditioning preserves mitochondrial function and activates pro-survival protein kinase Akt in the left ventricle during cardiac surgery: a randomized trial. Int J Cardiol. 2014;177:409–17.CrossRefPubMed
75.
Shimizu M, Konstantinov IE, Kharbanda RK, et al. Effects of intermittent lower limb ischaemia on coronary blood flow and coronary resistance in pigs. Acta Physiol (Oxf). 2007;190:103–9.CrossRef
76.
Zhou K, Yang B, Zhou XM, et al. Effects of remote ischemic preconditioning on the flow pattern of the left anterior descending coronary artery in normal subjects. Int J Cardiol. 2007;122:250–1.CrossRefPubMed
77.
McDonald MA, Braga JR, Li J, et al. A randomized pilot trial of remote ischemic preconditioning in heart failure with reduced ejection fraction. PLoS One. 2014;9:e105361.CrossRefPubMedPubMedCentral
78.
Seeger JP, Benda NM, Riksen NP, et al. Heart failure is associated with exaggerated endothelial ischaemia-reperfusion injury and attenuated effect of ischaemic preconditioning. Eur J Prev Cardiol. PMID: 25389072. doi:10.​1177/​2047487314558377​.
79.
Faselis C, Doumas M, Pittaras A, et al. Exercise capacity and all-cause mortality in male veterans with hypertension aged ≥70 years. Hypertension. 2014;64:30–5.CrossRefPubMed
80.
La Rovere MT, Pinna GD, Maestri R, et al. The 6-minute walking test and all-cause mortality in patients undergoing a post-cardiac surgery rehabilitation program. Eur J Prev Cardiol. 2015;22:20–6.CrossRefPubMed
81.
Myers J, Prakash M, Froelicher V, et al. Exercise capacity and mortality among men referred for exercise testing. N Engl J Med. 2002;346:793–801.CrossRefPubMed
82.
O’Connor CM, Whellan DJ, Wojdyla D, et al. Factors related to morbidity and mortality in patients with chronic heart failure with systolic dysfunction: the HF-ACTION predictive risk score model. Circ Heart Fail. 2012;5:63–71.CrossRefPubMedPubMedCentral
83.
Keteyian SJ, Leifer ES, Houston-Miller N, et al. Relation between volume of exercise and clinical outcomes in patients with heart failure. J Am Coll Cardiol. 2012;60:1899–905.CrossRefPubMedPubMedCentral
Metadata
Title
The Effects of Ischemic Preconditioning on Human Exercise Performance
Authors
Anthony V. Incognito
Jamie F. Burr
Philip J. Millar
Publication date
01-04-2016
Publisher
Springer International Publishing
Published in
Sports Medicine / Issue 4/2016
Print ISSN: 0112-1642
Electronic ISSN: 1179-2035
DOI
https://doi.org/10.1007/s40279-015-0433-5

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