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Published in: European Journal of Applied Physiology 1/2010

Open Access 01-01-2010 | Original Article

Ischemic preconditioning improves maximal performance in humans

Authors: Patricia C. E. de Groot, Dick H. J. Thijssen, Manuel Sanchez, Reinier Ellenkamp, Maria T. E. Hopman

Published in: European Journal of Applied Physiology | Issue 1/2010

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Abstract

Repeated episodes of ischemia followed by reperfusion, commonly referred to as ischemic preconditioning (IPC), represent an endogenous protective mechanism that delays cell injury. IPC also increases blood flow and improves endothelial function. We hypothesize that IPC will improve physical exercise performance and maximal oxygen consumption. The purpose of the study was to examine the effect of ischemic preconditioning in leg skeletal muscles on cycling exercise performance in healthy individuals. Fifteen healthy, well-trained subjects performed two incremental maximal exercise tests on a bicycle ergometer. Power output, oxygen consumption, ventilation, respiratory quotient, and heart rate were measured continuously. Blood pressure and blood lactate were measured before and after the test. One exercise test was performed after the application of ischemic preconditioning, using a protocol of three series of 5-min ischemia at both legs with resting periods of 5 min in between. The other maximal cycling test served as a control. Tests were conducted in counterbalanced order, at least 1 week apart, at the same time of the day. The repeated ischemic periods significantly increased maximal oxygen consumption from 56.8 to 58.4 ml/min per kg (P = 0.003). Maximal power output increased significantly from 366 to 372 W (P = 0.05). Ischemic preconditioning had no effect on ventilation, respiratory quotient, maximal heart rate, blood pressure or on blood lactate. Repeated short-term leg ischemia prior to an incremental bicycle exercise test improves maximal oxygen consumption by 3% and power output by 1.6%. This protocol, which is suggested to mimic the effects of ischemic preconditioning, may have important implications for exercise performance.
Literature
go back to reference Bushell AJ, Klenerman L, Taylor S, Davies H, Grierson I, Helliwell TR, Jackson MJ (2002) Ischaemic preconditioning of skeletal muscle. 1. Protection against the structural changes induced by ischaemia/reperfusion injury. J Bone Joint Surg Br 84:1184–1188CrossRefPubMed Bushell AJ, Klenerman L, Taylor S, Davies H, Grierson I, Helliwell TR, Jackson MJ (2002) Ischaemic preconditioning of skeletal muscle. 1. Protection against the structural changes induced by ischaemia/reperfusion injury. J Bone Joint Surg Br 84:1184–1188CrossRefPubMed
go back to reference Calbet JA, Lundby C, Sander M, Robach P, Saltin B, Boushel R (2006) Effects of ATP-induced leg vasodilation on VO2 peak and leg O2 extraction during maximal exercise in humans. Am J Physiol Regul Integr Comp Physiol 291:R447–R453PubMed Calbet JA, Lundby C, Sander M, Robach P, Saltin B, Boushel R (2006) Effects of ATP-induced leg vasodilation on VO2 peak and leg O2 extraction during maximal exercise in humans. Am J Physiol Regul Integr Comp Physiol 291:R447–R453PubMed
go back to reference Cooper CE, Brown GC (2008) The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: chemical mechanism and physiological significance. J Bioenerg Biomembr 40:533–539CrossRefPubMed Cooper CE, Brown GC (2008) The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: chemical mechanism and physiological significance. J Bioenerg Biomembr 40:533–539CrossRefPubMed
go back to reference Eisen A, Fisman EZ, Rubenfire M, Freimark D, McKechnie R, Tenenbaum A, Motro M, Adler Y (2004) Ischemic preconditioning: nearly two decades of research. A comprehensive review. Atherosclerosis 172:201–210CrossRefPubMed Eisen A, Fisman EZ, Rubenfire M, Freimark D, McKechnie R, Tenenbaum A, Motro M, Adler Y (2004) Ischemic preconditioning: nearly two decades of research. A comprehensive review. Atherosclerosis 172:201–210CrossRefPubMed
go back to reference Gross GJ, Auchampach JA (1992) Blockade of ATP-sensitive potassium channels prevents myocardial preconditioning in dogs. Circ Res 70:223–233PubMed Gross GJ, Auchampach JA (1992) Blockade of ATP-sensitive potassium channels prevents myocardial preconditioning in dogs. Circ Res 70:223–233PubMed
go back to reference Hopper RA, Forrest CR, Xu H, Zhong A, He W, Rutka J, Neligan P, Pang CY (2000) Role and mechanism of PKC in ischemic preconditioning of pig skeletal muscle against infarction. Am J Physiol Regul Integr Comp Physiol 279:R666–R676PubMed Hopper RA, Forrest CR, Xu H, Zhong A, He W, Rutka J, Neligan P, Pang CY (2000) Role and mechanism of PKC in ischemic preconditioning of pig skeletal muscle against infarction. Am J Physiol Regul Integr Comp Physiol 279:R666–R676PubMed
go back to reference Joyner MJ, Proctor DN (1999) Muscle blood flow during exercise: the limits of reductionism. Med Sci Sports Exerc 31:1036–1040CrossRefPubMed Joyner MJ, Proctor DN (1999) Muscle blood flow during exercise: the limits of reductionism. Med Sci Sports Exerc 31:1036–1040CrossRefPubMed
go back to reference Keller DM, Ogoh S, Greene S, Olivencia-Yurvati A, Raven PB (2004) Inhibition of KATP channel activity augments baroreflex-mediated vasoconstriction in exercising human skeletal muscle. J Physiol 561:273–282CrossRefPubMed Keller DM, Ogoh S, Greene S, Olivencia-Yurvati A, Raven PB (2004) Inhibition of KATP channel activity augments baroreflex-mediated vasoconstriction in exercising human skeletal muscle. J Physiol 561:273–282CrossRefPubMed
go back to reference Kimura M, Ueda K, Goto C, Jitsuiki D, Nishioka K, Umemura T, Noma K, Yoshizumi M, Chayama K, Higashi Y (2007) Repetition of ischemic preconditioning augments endothelium-dependent vasodilation in humans: role of endothelium-derived nitric oxide and endothelial progenitor cells. Arterioscler Thromb Vasc Biol 27:1403–1410CrossRefPubMed Kimura M, Ueda K, Goto C, Jitsuiki D, Nishioka K, Umemura T, Noma K, Yoshizumi M, Chayama K, Higashi Y (2007) Repetition of ischemic preconditioning augments endothelium-dependent vasodilation in humans: role of endothelium-derived nitric oxide and endothelial progenitor cells. Arterioscler Thromb Vasc Biol 27:1403–1410CrossRefPubMed
go back to reference Kooijman M, Thijssen DH, de Groot PC, Bleeker MW, van Kuppevelt HJ, Green DJ, Rongen GA, Smits P, Hopman MT (2008) Flow-mediated dilatation in the superficial femoral artery is nitric oxide mediated in humans. J Physiol 586:1137–1145CrossRefPubMed Kooijman M, Thijssen DH, de Groot PC, Bleeker MW, van Kuppevelt HJ, Green DJ, Rongen GA, Smits P, Hopman MT (2008) Flow-mediated dilatation in the superficial femoral artery is nitric oxide mediated in humans. J Physiol 586:1137–1145CrossRefPubMed
go back to reference Lawson CS, Downey JM (1993) Preconditioning: state of the art myocardial protection. Cardiovasc Res 27:542–550CrossRefPubMed Lawson CS, Downey JM (1993) Preconditioning: state of the art myocardial protection. Cardiovasc Res 27:542–550CrossRefPubMed
go back to reference Levine BD, Stray-Gundersen J (1997) Living high-training low: effect of moderate-altitude acclimatization with low-altitude training on performance. J Appl Physiol 83:102–112PubMed Levine BD, Stray-Gundersen J (1997) Living high-training low: effect of moderate-altitude acclimatization with low-altitude training on performance. J Appl Physiol 83:102–112PubMed
go back to reference Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124–1136PubMed Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124–1136PubMed
go back to reference Pang CY, Yang RZ, Zhong A, Xu N, Boyd B, Forrest CR (1995) Acute ischaemic preconditioning protects against skeletal muscle infarction in the pig. Cardiovasc Res 29:782–788PubMed Pang CY, Yang RZ, Zhong A, Xu N, Boyd B, Forrest CR (1995) Acute ischaemic preconditioning protects against skeletal muscle infarction in the pig. Cardiovasc Res 29:782–788PubMed
go back to reference Pang CY, Neligan P, Xu H, He W, Zhong A, Hopper R, Forrest CR (1997) Role of ATP-sensitive K+ channels in ischemic preconditioning of skeletal muscle against infarction. Am J Physiol 273:H44–H51PubMed Pang CY, Neligan P, Xu H, He W, Zhong A, Hopper R, Forrest CR (1997) Role of ATP-sensitive K+ channels in ischemic preconditioning of skeletal muscle against infarction. Am J Physiol 273:H44–H51PubMed
go back to reference Prime TA, Blaikie FH, Evans C, Nadtochiy SM, James AM, Dahm CC, Vitturi DA, Patel RP, Hiley CR, Abakumova I, Requejo R, Chouchani ET, Hurd TR, Garvey JF, Taylor CT, Brookes PS, Smith RA, Murphy MP (2009) A mitochondria-targeted S-nitrosothiol modulates respiration, nitrosates thiols, and protects against ischemia-reperfusion injury. Proc Natl Acad Sci USA 106(26):10764–10769 Prime TA, Blaikie FH, Evans C, Nadtochiy SM, James AM, Dahm CC, Vitturi DA, Patel RP, Hiley CR, Abakumova I, Requejo R, Chouchani ET, Hurd TR, Garvey JF, Taylor CT, Brookes PS, Smith RA, Murphy MP (2009) A mitochondria-targeted S-nitrosothiol modulates respiration, nitrosates thiols, and protects against ischemia-reperfusion injury. Proc Natl Acad Sci USA 106(26):10764–10769
go back to reference Reimer KA, Murry CE, Yamasawa I, Hill ML, Jennings RB (1986) Four brief periods of myocardial ischemia cause no cumulative ATP loss or necrosis. Am J Physiol 251:H1306–H1315PubMed Reimer KA, Murry CE, Yamasawa I, Hill ML, Jennings RB (1986) Four brief periods of myocardial ischemia cause no cumulative ATP loss or necrosis. Am J Physiol 251:H1306–H1315PubMed
go back to reference Rubio R, Ceballos G, Balcells E (1999) Intravascular adenosine: the endothelial mediators of its negative dromotropic effects. Eur J Pharmacol 370:27–37CrossRefPubMed Rubio R, Ceballos G, Balcells E (1999) Intravascular adenosine: the endothelial mediators of its negative dromotropic effects. Eur J Pharmacol 370:27–37CrossRefPubMed
go back to reference Saito T, Komiyama T, Aramoto H, Miyata T, Shigematsu H (2004) Ischemic preconditioning improves oxygenation of exercising muscle in vivo. J Surg Res 120:111–118CrossRefPubMed Saito T, Komiyama T, Aramoto H, Miyata T, Shigematsu H (2004) Ischemic preconditioning improves oxygenation of exercising muscle in vivo. J Surg Res 120:111–118CrossRefPubMed
go back to reference Schroeder CA Jr, Lee HT, Shah PM, Babu SC, Thompson CI, Belloni FL (1996) Preconditioning with ischemia or adenosine protects skeletal muscle from ischemic tissue reperfusion injury. J Surg Res 63:29–34CrossRefPubMed Schroeder CA Jr, Lee HT, Shah PM, Babu SC, Thompson CI, Belloni FL (1996) Preconditioning with ischemia or adenosine protects skeletal muscle from ischemic tissue reperfusion injury. J Surg Res 63:29–34CrossRefPubMed
go back to reference Stray-Gundersen J, Chapman RF, Levine BD (2001) Living high-training low altitude training improves sea level performance in male and female elite runners. J Appl Physiol 91:1113–1120PubMed Stray-Gundersen J, Chapman RF, Levine BD (2001) Living high-training low altitude training improves sea level performance in male and female elite runners. J Appl Physiol 91:1113–1120PubMed
go back to reference Todd J, Zhao ZQ, Williams MW, Sato H, Van Wylen DG, Vinten-Johansen J (1996) Intravascular adenosine at reperfusion reduces infarct size and neutrophil adherence. Ann Thorac Surg 62:1364–1372CrossRefPubMed Todd J, Zhao ZQ, Williams MW, Sato H, Van Wylen DG, Vinten-Johansen J (1996) Intravascular adenosine at reperfusion reduces infarct size and neutrophil adherence. Ann Thorac Surg 62:1364–1372CrossRefPubMed
go back to reference Weselcouch EO, Sargent C, Wilde MW, Smith MA (1993) ATP-sensitive potassium channels and skeletal muscle function in vitro. J Pharmacol Exp Ther 267:410–416PubMed Weselcouch EO, Sargent C, Wilde MW, Smith MA (1993) ATP-sensitive potassium channels and skeletal muscle function in vitro. J Pharmacol Exp Ther 267:410–416PubMed
Metadata
Title
Ischemic preconditioning improves maximal performance in humans
Authors
Patricia C. E. de Groot
Dick H. J. Thijssen
Manuel Sanchez
Reinier Ellenkamp
Maria T. E. Hopman
Publication date
01-01-2010
Publisher
Springer-Verlag
Published in
European Journal of Applied Physiology / Issue 1/2010
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-009-1195-2

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