Download PDF
Int J Sports Med 2016; 37(02): 87-96
DOI: 10.1055/s-0035-1564253
Review
© Georg Thieme Verlag KG Stuttgart · New York

Myths and Facts About the Effects of Ischemic Preconditioning on Performance

M. Marocolo
1   Human Performance and Sport Research Group, Department of Sport Sciences, Federal University of Triângulo Mineiro, Uberaba, Brazil
2   German Sport University, Physiology & Anatomy, Cologne
,
G. R. da Mota
1   Human Performance and Sport Research Group, Department of Sport Sciences, Federal University of Triângulo Mineiro, Uberaba, Brazil
,
M. A. M. Simim
1   Human Performance and Sport Research Group, Department of Sport Sciences, Federal University of Triângulo Mineiro, Uberaba, Brazil
,
H.-J. Appell Coriolano
2   German Sport University, Physiology & Anatomy, Cologne
› Author Affiliations
Further Information

Publication History



accepted after revision 14 September 2015

Publication Date:
28 October 2015 (online)

Also available at
    Permissions and Reprints

Corrected by:

Myths and Facts About the Effects of Ischemic Preconditioning on PerformanceInt J Sports Med 2016; 37(02): e7-e7
DOI: 10.1055/s-0035-1565185

Abstract

Although numerous studies have demonstrated the effect of ischemic preconditioning (IPC) in clinical application, the effectiveness of this procedure on performance and physiological variables is still debatable. Therefore a systematic review was performed, including a meta-analysis and evaluation of the quality of the papers that addressed this scope. The electronic databases of the National Library of Medicine (PubMed), Google Scholar (using [advanced search], [all fields]) and other online journals were searched, for the following descriptors: a) “ischemic preconditioning”; b) “blood flow” and “hyperemia”; c) “blood flow occlusion,” combined with “exercise performance”, “athletes”, “exercise” and “performance”. Relevant studies were included, if they conformed to strict pre-formulated criteria, excluding systematic review articles, meta-analyses and studies with only animals or non-healthy subjects. The 20 studies included had high quality scores (87%). The majority of the studies lacked statistical significance (P<0.05) for both performance and physiological variables when comparing IPC, placebo and control groups. Most studies showed that IPC has no significant influence on performance. The few studies with significant differences mainly described an improvement only in performance without altered physiological parameters. Therefore, the influence of IPC on performance is still unclear and physiologically highly debatable.

Key words

blood flow occlusion - hyperemia - sports - testing
 

  • References

  • 1 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: 2084-2089
    CrossrefPubMedSearch in Google Scholar
  • 2 Barbosa TC, Machado AC, Braz ID, Fernandes IA, Vianna LC, Nobrega AC, Silva BM. Remote ischemic preconditioning delays fatigue development during handgrip exercise. Scand J Med Sci Sports 2014;
    PubMedSearch in Google Scholar
  • 3 Barcroft H, Lind AR, Petrofsky JS. The lack of influence of reactive hyperemia on exhausting rhythmic or static exercise. Eur J Appl Physiol 1978; 38: 49-54
    CrossrefPubMedSearch in Google Scholar
  • 4 Barr MW. The Effect of Ischemic Preconditioning on Repeated Supramaximal Sprints [Master]. Ohio University 2011: 68
    PubMedSearch in Google Scholar
  • 5 Batterham AM, Hopkins WG. Making meaningful inferences about magnitudes. Int J Sports Physiol Perform 2006; 1: 50-57
    PubMedSearch in Google Scholar
  • 6 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: 1132-1139
    CrossrefPubMedSearch in Google Scholar
  • 7 Cheung MM, Kharbanda RK, Konstantinov IE, Shimizu M, Frndova H, Li J, Holtby HM, Cox PN, Smallhorn JF, Van Arsdell GS, Redington AN. Randomized controlled trial of the effects of remote ischemic preconditioning on children undergoing cardiac surgery: first clinical application in humans. J Am Coll Cardiol 2006; 47: 2277-2282
    CrossrefPubMedSearch in Google Scholar
  • 8 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: 3649-3654
    CrossrefPubMedSearch in Google Scholar
  • 9 Cochran WG. The combination of estimates from different experiments. Biometrics 1954; 10: 101-129
    CrossrefPubMedSearch in Google Scholar
  • 10 Cochrane DJ, Booker HR, Mundel T, Barnes MJ. Does intermittent pneumatic leg compression enhance muscle recovery after strenuous eccentric exercise?. Int J Sports Med 2013; 34: 969-974
    Thieme ConnectPubMedSearch in Google Scholar
  • 11 Cohen J. Statistical Power Analysis for the Behavioural Sciences. 2nd ed. Hillsdale, NJ: Lawrence Erlbaum; 1988
    Search in Google Scholar
  • 12 Collier EAPCJ. The working capacity of muscle during reactive hyperemia. Ergonomics 1959; 2: 114-118
    PubMedSearch in Google Scholar
  • 13 Cormie P, McGuigan MR, Newton RU. Developing maximal neuromuscular power: Part 2-training considerations for improving maximal power production. Sports Med 2011; 41: 125-146
    CrossrefPubMedSearch in Google Scholar
  • 14 Crisafulli A, Tangianu F, Tocco F, Concu A, Mameli O, Mulliri G, Caria MA. Ischemic preconditioning of the muscle improves maximal exercise performance but not maximal oxygen uptake in humans. J Appl Physiol 2011; 111: 530-536
    CrossrefPubMedSearch in Google Scholar
  • 15 de Groot PC, Thijssen DH, Sanchez M, Ellenkamp R, Hopman MT. Ischemic preconditioning improves maximal performance in humans. Eur J Appl Physiol 2010; 108: 141-146
    CrossrefPubMedSearch in Google Scholar
  • 16 Dickson EW, Reinhardt CP, Renzi FP, Becker RC, Porcaro WA, Heard SO. Ischemic preconditioning may be transferable via whole blood transfusion: preliminary evidence. J Thromb Thrombolysis 1999; 8: 123-129
    CrossrefPubMedSearch in Google Scholar
  • 17 Ding YF, Zhang MM, He RR. Ischemic preconditioning reduces cardiomyocytic apoptosis in rabbit heart in vivo. Sheng Li Xue Bao 2000; 52: 220-224
    PubMedSearch in Google Scholar
  • 18 Downs S, Black N. The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Commun Health 1998; 52: 377-384
    CrossrefPubMedSearch in Google Scholar
  • 19 Eisen A, Fisman EZ, Rubenfire M, Freimark D, McKechnie R, Tenenbaum A, Motro M, Adler Y. Ischemic preconditioning: nearly two decades of research. A comprehensive review. Atherosclerosis 2004; 172: 201-210
    CrossrefPubMedSearch in Google Scholar
  • 20 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: 155-161
    CrossrefPubMedSearch in Google Scholar
  • 21 Foster GP, Westerdahl DE, Foster LA, Hsu JV, Anholm JD. Ischemic preconditioning of the lower extremity attenuates the normal hypoxic increase in pulmonary artery systolic pressure. Respir Physiol Neurobiol 2011; 179: 248-253
    CrossrefPubMedSearch in Google Scholar
  • 22 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 2014; 1-7
    PubMedSearch in Google Scholar
  • 23 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: 671-676
    PubMedSearch in Google Scholar
  • 24 Hagar JM, Hale SL, Kloner RA. Effect of preconditioning ischemia on reperfusion arrhythmias after coronary artery occlusion and reperfusion in the rat. Circ Res 1991; 68: 61-68
    CrossrefPubMedSearch in Google Scholar
  • 25 Hajrasouliha AR, Tavakoli S, Ghasemi M, Jabehdar-Maralani P, Sadeghipour H, Ebrahimi F, Dehpour AR. Endogenous cannabinoids contribute to remote ischemic preconditioning via cannabinoid CB2 receptors in the rat heart. Eur J Pharmacol 2008; 579: 246-252
    CrossrefPubMedSearch in Google Scholar
  • 26 Higgins JPT, Thompson SG. Quantifying heterogeneity in a metaanalysis. Stat Med 2002; 21: 1539-1558
    CrossrefPubMedSearch in Google Scholar
  • 27 Hittinger EA, Maher JL, Nash MS, Perry AC, Signorile JF, Kressler J, Jacobs KA. 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
    CrossrefPubMedSearch in Google Scholar
  • 28 Hong DM, Jeon Y, Lee CS, Kim HJ, Lee JM, Bahk JH, Kim KB, Hwang HY. Effects of remote ischemic preconditioning with postconditioning in patients undergoing off-pump coronary artery bypass surgery – randomized controlled trial. Circ J 2012; 76: 884-890
    CrossrefPubMedSearch in Google Scholar
  • 29 Howell AK, Gaughan JP, Cairns MA, Faigenbaum AD, Libonati JR. The effect of muscle hypoperfusion-hyperemia on repetitive vertical jump performance. J Strength Cond Res 2001; 15: 446-449
    PubMedSearch in Google Scholar
  • 30 Hu S, Dong HL, Li YZ, Luo ZJ, Sun L, Yang QZ, Yang LF, Xiong L. Effects of remote ischemic preconditioning on biochemical markers and neurologic outcomes in patients undergoing elective cervical decompression surgery: a prospective randomized controlled trial. J Neurosurg Anesthesiol 2010; 22: 46-52
    CrossrefPubMedSearch in Google Scholar
  • 31 Janier MF, Vanoverschelde JL, Bergmann SR. Ischemic preconditioning stimulates anaerobic glycolysis in the isolated rabbit heart. Am J Physiol 1994; 267: H1353-H1360
    PubMedSearch in Google Scholar
  • 32 Jean-St-Michel E, Manlhiot C, Li J, Tropak M, Michelsen MM, Schmidt MR, McCrindle BW, Wells GD, Redington AN. Remote preconditioning improves maximal performance in highly trained athletes. Med Sci Sports Exerc 2011; 43: 1280-1286
    CrossrefPubMedSearch in Google Scholar
  • 33 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: 151-155
    PubMedSearch in Google Scholar
  • 34 Kocman EA, Ozatik O, Sahin A, Guney T, Kose AA, Dag I, Alatas O, Cetin C. Effects of ischemic preconditioning protocols on skeletal muscle ischemia-reperfusion injury. J Surg Res 2015; 193: 942-952
    CrossrefPubMedSearch in Google Scholar
  • 35 Kraemer WJ, Noble BJ, Clark MJ, Culver BW. Physiologic responses to heavy-resistance exercise with very short rest periods. Int J Sports Med 1987; 8: 247-252
    Thieme ConnectPubMedSearch in Google Scholar
  • 36 Lalonde F, Curnier DY. Can anaerobic performance be improved by remote ischemic preconditioning?. J Strength Cond Res 2015; 29: 80-85
    CrossrefPubMedSearch in Google Scholar
  • 37 Libonati JR, Cox M, Incanno N, Melville SK, Musante FC, Glassberg HL, Guazzi M. Brief periods of occlusion and reperfusion increase skeletal muscle force output in humans. Cardiologia 1998; 43: 1355-1360
    PubMedSearch in Google Scholar
  • 38 Libonati JR, Howell AK, Incanno NM, Pettee KK, Glassberg HL. Brief muscle hypoperfusion/hyperemia: an ergogenic aid?. J Strength Cond Res 2001; 15: 362-366
    PubMedSearch in Google Scholar
  • 39 Lott FD, Guo P, Toombs CF. Reduction in infarct size by ischemic preconditioning persists in a chronic rat model of myocardial ischemia-reperfusion injury. Pharmacology 1996; 52: 113-118
    CrossrefPubMedSearch in Google Scholar
  • 40 Marocolo M, da Mota GR, Pelegrini V, Appell Coriolano HJ. Are the beneficial effects of ischemic preconditioning on performance partly a placebo effect?. Int J Sports Med 2015; 36: 822-825
    Thieme ConnectPubMedSearch in Google Scholar
  • 41 Mendez-Villanueva A, Edge J, Suriano R, Hamer P, Bishop D. The recovery of repeated-sprint exercise is associated with PCr resynthesis, while muscle pH and EMG amplitude remain depressed. PLoS One 2012; 7: e51977
    CrossrefPubMedSearch in Google Scholar
  • 42 Muller EA. Muscular work and muscular blood circulation in reactive hyperemia. Pflugers Arch 1958; 265: 29-39
    PubMedSearch in Google Scholar
  • 43 Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986; 74: 1124-1136
    CrossrefPubMedSearch in Google Scholar
  • 44 Nukada A. Muscular performance in reactive hyperemia of muscles. Int Z Angew Physiol 1955; 16: 81-82
    PubMedSearch in Google Scholar
  • 45 Ovize M, Thibault H, Przyklenk K. Myocardial conditioning: opportunities for clinical translation. Circ Res 2013; 113: 439-450
    CrossrefPubMedSearch in Google Scholar
  • 46 Paixao RC, da Mota GR, Marocolo M. Acute effect of ischemic preconditioning is detrimental to anaerobic performance in cyclists. Int J Sports Med 2014; 35: 912-915
    Thieme ConnectPubMedSearch in Google Scholar
  • 47 Patel HH, Moore J, Hsu AK, Gross GJ. Cardioprotection at a distance: mesenteric artery occlusion protects the myocardium via an opioid sensitive mechanism. J Mol Cell Cardiol 2002; 34: 1317-1323
    CrossrefPubMedSearch in Google Scholar
  • 48 Patterson SD, Bezodis NE, Glaister M, Pattison JR. The effect of ischemic preconditioning on repeated sprint cycling performance. Med Sci Sports Exerc. 2014
    PubMedSearch in Google Scholar
  • 49 Pell TJ, Baxter GF, Yellon DM, Drew GM. Renal ischemia preconditions myocardium: role of adenosine receptors and ATP-sensitive potassium channels. Am J Physiol 1998; 275: H1542-H1547
    PubMedSearch in Google Scholar
  • 50 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: 893-899
    CrossrefPubMedSearch in Google Scholar
  • 51 Robergs RA, Pearson DR, Costill DL, Fink WJ, Pascoe DD, Benedict MA, Lambert CP, Zachweija JJ. Muscle glycogenolysis during differing intensities of weight-resistance exercise. J Appl Physiol 1991; 70: 1700-1706
    PubMedSearch in Google Scholar
  • 52 Schoemaker RG, van Heijningen CL. Bradykinin mediates cardiac preconditioning at a distance. Am J Physiol 2000; 278: H1571-H1576
    PubMedSearch in Google Scholar
  • 53 Singh D, Chopra K. Evidence of the role of angiotensin AT(1) receptors in remote renal preconditioning of myocardium. Methods Find Exp Clin Pharmacol 2004; 26: 117-122
    CrossrefPubMedSearch in Google Scholar
  • 54 Slagsvold KH, Rognmo O, Hoydal M, Wisloff U, Wahba A. Remote ischemic preconditioning preserves mitochondrial function and influences myocardial microRNA expression in atrial myocardium during coronary bypass surgery. Circ Res 2014; 114: 851-859
    CrossrefPubMedSearch in Google Scholar
  • 55 Tang ZL, Dai W, Li YJ, Deng HW. Involvement of capsaicin-sensitive sensory nerves in early and delayed cardioprotection induced by a brief ischaemia of the small intestine. Naunyn Schmiedebergs Arch Pharmacol 1999; 359: 243-247
    CrossrefPubMedSearch in Google Scholar
  • 56 Tocco F, Marongiu E, Ghiani G, Sanna I, Palazzolo G, Olla S, Pusceddu M, Sanna P, Corona F, Concu A, Crisafulli A. Muscle ischemic preconditioning does not improve performance during self-paced exercise. Int J Sports Med 2015; 36: 9-15
    Thieme ConnectPubMedSearch in Google Scholar
  • 57 van Velzen JM, van Bennekom CAM, Polomski W, Slootman JR, van der Woude LHV, Houdijk H. Physical capacity and walking ability after lower limb amputation: a systematic review. Clin Rehabil 2006; 20: 999-1016
    CrossrefPubMedSearch in Google Scholar
  • 58 Weinbrenner C, Nelles M, Herzog N, Sarvary L, Strasser RH. Remote preconditioning by infrarenal occlusion of the aorta protects the heart from infarction: a newly identified non-neuronal but PKC-dependent pathway. Cardiovasc Res 2002; 55: 590-601
    CrossrefPubMedSearch in Google Scholar
  • 59 Wolfrum S, Nienstedt J, Heidbreder M, Schneider K, Dominiak P, Dendorfer A. Calcitonin gene related peptide mediates cardioprotection by remote preconditioning. Regul Pept 2005; 127: 217-224
    CrossrefPubMedSearch in Google Scholar
  • 60 Yamashita N, Hoshida S, Taniguchi N, Kuzuya T, Hori M. A “second window of protection” occurs 24 h after ischemic preconditioning in the rat heart. J Mol Cell Cardiol 1998; 30: 1181-1189
    CrossrefPubMedSearch in Google Scholar
  • 61 Zaykin DV. Optimally weighted Z-test is a powerful method for combining probabilities in meta-analysis. J Evol Biol 2011; 24: 1836-1841
    CrossrefPubMedSearch in Google Scholar