Download PDF
Int J Sports Med 2018; 39(08): 596-603
DOI: 10.1055/a-0631-2887
Physiology & Biochemistry
© Georg Thieme Verlag KG Stuttgart · New York

Ischemic Preconditioning Enhances Performance and Erythrocyte Deformability of Responders

Fabian Tomschi
1   German Sport University Cologne, Molecular and Cellular Sports Medicine, Cologne, Germany
,
David Niemann
1   German Sport University Cologne, Molecular and Cellular Sports Medicine, Cologne, Germany
,
Wilhelm Bloch
1   German Sport University Cologne, Molecular and Cellular Sports Medicine, Cologne, Germany
,
Hans-Georg Predel
2   German Sport University Cologne, Institute of Cardiology and Sports Medicine, Cologne, Germany
,
Marijke Grau
1   German Sport University Cologne, Molecular and Cellular Sports Medicine, Cologne, Germany
› Author Affiliations
Further Information

Publication History



accepted 11 April 2018

Publication Date:
08 June 2018 (online)

Also available at
    Permissions and Reprints

Abstract

This pilot study aimed to evaluate the differential effects of a remote ischemic preconditioning (rIPC) manoeuvre on performance and red blood cell (RBC) deformability compared to a sham control and a placebo setting. Ten male subjects performed three test settings in a single-blind, crossover, and randomized control design. All settings started with 20 min of rest and were followed by 4 cycles of occlusion/reperfusion consisting of 5 min each. During rIPC and placebo, the cuff pressure was inflated to 200 mmHg and 120 mmHg, respectively. During the sham control setting, 10 mmHg pressure was applied. All tests were followed by a cycle exercise with lactate diagnostics. Power at 2 and 4 mmol/l lactate thresholds were calculated. RBC deformability was measured before and after the respective manoeuvre. Results showed that no effect resulted from any manoeuvre on performance values or RBC deformability. But 6 subjects showed a higher power at the 2 mmol/l threshold, and 5 subjects exerted higher power at the 4 mmol/l threshold when the rIPC manoeuvre preceded the exercise. In these responsive subjects, RBC deformability also improved. Hence, rIPC effects are much influenced by the subjects’ responsiveness, and improved RBC deformability might contribute to enhanced performance in responsive subjects.

Key words

remote ischemic preconditioning - red blood cells - performance - lactate - deformability - cycling
 

  • References

  • 1 Addison PD, Neligan PC, Ashrafpour H, Khan A, Zhong A, Moses M, Forrest CR, Pang CY. Noninvasive remote ischemic preconditioning for global protection of skeletal muscle against infarction. Am J Physiol Heart Circ Physiol 2003; 285: H1435-H1443
    CrossrefPubMedGoogle Scholar
  • 2 Bailey TG, Jones H, Gregson W, Atkinson G, Cable NT, Thijssen DHJ. Effect of ischemic preconditioning on lactate accumulation and running performance. Med Sci Sports Exerc 2012; 44: 2084-2089
    CrossrefPubMedGoogle Scholar
  • 3 Barbosa TC, Machado AC, Braz ID, Fernandes IA, Vianna LC, Nobrega ACL, Silva BM. Remote ischemic preconditioning delays fatigue development during handgrip exercise. Scand J Med Sci Sports 2015; 25: 356-364
    CrossrefPubMedGoogle Scholar
  • 4 Baskurt OK, Hardeman MR, Uyuklu M, Ulker P, Cengiz M, Nemeth N, Shin S, Alexy T, Meiselman HJ. Parameterization of red blood cell elongation index – shear stress curves obtained by ektacytometry. Scand J Clin Lab Invest Suppl 2009; 69: 777-788
    CrossrefPubMedGoogle Scholar
  • 5 Baum BS, Li L. Lower extremity muscle activities during cycling are influenced by load and frequency. J Electromyogr Kinesiol 2003; 13: 181-190
    CrossrefPubMedGoogle Scholar
  • 6 Bijker KE, de Groot G, Hollander AP. Differences in leg muscle activity during running and cycling in humans. Eur J Appl Physiol 2002; 87: 556-561
    CrossrefPubMedGoogle Scholar
  • 7 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
    CrossrefPubMedGoogle Scholar
  • 8 Connes P, Tripette J, Mukisi-Mukaza M, Baskurt OK, Toth K, Meiselman HJ, Hue O, Antoine-Jonville S. Relationships between hemodynamic, hemorheological and metabolic responses during exercise. Biorheology 2009; 46: 133-143
    CrossrefPubMedGoogle Scholar
  • 9 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
    CrossrefPubMedGoogle Scholar
  • 10 Cruz RS, de Aguiar RA, Turnes T, Pereira KL, Caputo F. Effects of ischemic preconditioning on maximal constant-load cycling performance. J Appl Physiol 2015; 119: 961-967
    CrossrefPubMedGoogle Scholar
  • 11 da Mota GR, Marocolo M. The effects of ischemic preconditioning on human exercise performance: a counterpoint. Sports Med 2016; 46: 1575-1576
    CrossrefPubMedGoogle Scholar
  • 12 Enko K, Nakamura K, Yunoki K, Miyoshi T, Akagi S, Yoshida M, Toh N, Sangawa M, Nishii N, Nagase S, Kohno K, Morita H, Kusano KF, Ito H. Intermittent arm ischemia induces vasodilatation of the contralateral upper limb. J Physiol Sci 2011; 61: 507-513
    CrossrefPubMedGoogle Scholar
  • 13 Ferreira TN, Sabino-Carvalho JL, Lopes TR, Ribeiro IC, Succi JE, Da Silva AC, Silva BM. Ischemic preconditioning and repeated sprint swimming. A placebo and nocebo study. Med Sci Sports Exerc 2016; 48: 1967-1975
    CrossrefPubMedGoogle Scholar
  • 14 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
    CrossrefPubMedGoogle Scholar
  • 15 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: 1182-1188
    CrossrefPubMedGoogle Scholar
  • 16 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
    CrossrefPubMedGoogle Scholar
  • 17 Grau M, Kollikowski A, Bloch W. Remote ischemia preconditioning increases red blood cell deformability through red blood cell-nitric oxide synthase activation. Clin Hemorheol Microcirc 2016; 63: 185-197
    PubMedGoogle Scholar
  • 18 Grau M, Pauly S, Ali J, Walpurgis K, Thevis M, Bloch W, Suhr F. RBC-NOS-dependent S-nitrosylation of cytoskeletal proteins improves RBC deformability. PLoS One 2013; 8: e56759
    CrossrefPubMedGoogle Scholar
  • 19 Griffin PJ, Ferguson RA, Gissane C, Bailey SJ, Patterson SD. Ischemic preconditioning enhances critical power during a 3 minute all-out cycling test. J Sports Sci 2018; 36: 1038-1043
    CrossrefPubMedGoogle Scholar
  • 20 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
    CrossrefPubMedGoogle Scholar
  • 21 Hardeman MR, Dobbe JG, Ince C. The laser-assisted optical rotational cell analyzer (LORCA) as red blood cell aggregometer. Clin Hemorheol Microcirc 2001; 25: 1-11
    PubMedGoogle Scholar
  • 22 Harriss DJ, Macsween A, Atkinson G. Standards for ethics in sport and exercise science research: 2018 update. Int J Sports Med 2017; 38: 1126-1131
    Article in Thieme ConnectPubMedGoogle Scholar
  • 23 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
    CrossrefPubMedGoogle Scholar
  • 24 Horiuchi M. Ischemic preconditioning. Potential impact on exercise performance and underlying mechanisms. J Phys Fitness Sports Med 2017; 6: 15-23
    PubMedGoogle Scholar
  • 25 Horiuchi M, Endo J, Thijssen DH. Impact of ischemic preconditioning on functional sympatholysis during handgrip exercise in humans. Physiol Rep 2015; 3: e12304
    CrossrefPubMedGoogle Scholar
  • 26 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
    PubMedGoogle Scholar
  • 27 Incognito AV, Burr JF, Millar PJ. The effects of ischemic preconditioning on human exercise performance. Sports Med 2016; 46: 531-544
    CrossrefPubMedGoogle Scholar
  • 28 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
    CrossrefPubMedGoogle Scholar
  • 29 Jones H, Nyakayiru J, Bailey TG, Green DJ, Cable NT, Sprung VS, Hopkins ND, Thijssen DHJ. Impact of eight weeks of repeated ischaemic preconditioning on brachial artery and cutaneous microcirculatory function in healthy males. Eur J Prev Cardiol 2015; 22: 1083-1087
    CrossrefPubMedGoogle Scholar
  • 30 Jung C, Jung F, Kelm M. The microcirculation in hypoxia: The center of the battlefield for oxygen. Clin Hemorheol Microcirc 2016; 63: 169-172
    PubMedGoogle Scholar
  • 31 Kido K, Suga T, Tanaka D, Honjo T, Homma T, Fujita S, Hamaoka T, Isaka T. Ischemic preconditioning accelerates muscle deoxygenation dynamics and enhances exercise endurance during the work-to-work test. Physiol Rep 2015; 3: e12395
    CrossrefPubMedGoogle Scholar
  • 32 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
    PubMedGoogle Scholar
  • 33 Koch S, Della-Morte D, Dave KR, Sacco RL, Perez-Pinzon MA. Biomarkers for ischemic preconditioning: finding the responders. Cereb Blood Flow Metab 2014; 34: 933-941
    PubMedGoogle Scholar
  • 34 Lalonde F, Curnier DY. Can anaerobic performance be improved by remote ischemic preconditioning?. J Strength Cond Res 2015; 29: 80-85
    CrossrefPubMedGoogle Scholar
  • 35 Leva Pd. Adjustments to Zatsiorsky-Seluyanov's segment inertia parameters. J Biomech 1996; 29: 1223-1230
    CrossrefPubMedGoogle Scholar
  • 36 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
    PubMedGoogle Scholar
  • 37 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
    PubMedGoogle Scholar
  • 38 Lindsay A, Petersen C, Blackwell G, Ferguson H, Parker G, Steyn N, Gieseg SP. The effect of 1 week of repeated ischaemic leg preconditioning on simulated Keirin cycling performance. A randomised trial. BMJ Open Sport Exerc Med 2017; 3: e000229
    PubMedGoogle Scholar
  • 39 Lintz JA, Dalio MB, Joviliano EE, Piccinato CE. Ischemic pre- and postconditioning in skeletal muscle injury produced by ischemia and reperfusion in rats. Acta Cir Bra 2013; 28: 441-446
    PubMedGoogle Scholar
  • 40 Lisbôa FD, Turnes T, Cruz RS, Raimundo JA, Pereira GS, Caputo F. The time dependence of the effect of ischemic preconditioning on successive sprint swimming performance. J Sci Med Sport 2017; 5: 507-511
    PubMedGoogle Scholar
  • 41 Mairbäurl H. Red blood cells in sports. Effects of exercise and training on oxygen supply by red blood cells. Front Physiol 2013; 4: 1-13
    PubMedGoogle Scholar
  • 42 Marocolo IC, da Mota GR, Londe AM, Patterson SD, Barbosa Neto O, Marocolo M. Acute ischemic preconditioning does not influence high-intensity intermittent exercise performance. Peer J 2017; 5: e4118
    CrossrefPubMedGoogle Scholar
  • 43 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
    Article in Thieme ConnectPubMedGoogle Scholar
  • 44 Marocolo M, da Mota GR, Simim MAM, Appell Coriolano HJ. Myths and facts about the effects of ischemic preconditioning on performance. Int J Sports Med 2016; 37: 87-96
    Article in Thieme ConnectPubMedGoogle Scholar
  • 45 Marocolo M, Willardson JM, Marocolo IC, da Mota GR, Simão R, Maior AS. Ischemic preconditioning and placebo intervention improves resistance exercise performance. J Strength Cond Res 2016; 30: 1462-1469
    CrossrefPubMedGoogle Scholar
  • 46 Muller EA. Muscular work and muscular blood circulation in reactive hyperemia. Pflugers Arch 1958; 265: 29-39
    PubMedGoogle Scholar
  • 47 Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium. Circulation 1986; 74: 1124-1136
    CrossrefPubMedGoogle Scholar
  • 48 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: 912-915
    Article in Thieme ConnectPubMedGoogle Scholar
  • 49 Pang CY, Yang RZ, Zhong A, Xu N, Boyd B, Forrest CR. Acute ischaemic preconditioning protects against skeletal muscle infarction in the pig. Cardiovasc Res 1995; 29: 782-788
    CrossrefPubMedGoogle Scholar
  • 50 Paradis-Deschênes P, Joanisse DR, Billaut F. Sex-specific impact of ischemic preconditioning on tissue oxygenation and maximal concentric force. Front Psychol 2016; 7: 674
    PubMedGoogle Scholar
  • 51 Patterson SD, Bezodis NE, Glaister M, Pattison JR. The effect of ischemic preconditioning on repeated sprint cycling performance. Med Sci Sports Exerc 2015; 47: 1652-1658
    CrossrefPubMedGoogle Scholar
  • 52 Smith JA, Martin DT, Telford RD, Ballas SK. Greater erythrocyte deformability in world-class endurance athletes. Am J Physiol 1999; 276: H2188-H2193
    PubMedGoogle Scholar
  • 53 Suhr F, Brenig J, Muller R, Behrens H, Bloch W, Grau M. Moderate exercise promotes human RBC-NOS activity, NO production and deformability through Akt kinase pathway. PLoS One 2012; 7: e45982
    CrossrefPubMedGoogle Scholar
  • 54 Tanaka D, Suga T, Tanaka T, Kido K, Honjo T, Fujita S, Hamaoka T, Isaka T. Ischemic preconditioning enhances muscle endurance during sustained isometric exercise. Int J Sports Med 2016; 37: 614-618
    Article in Thieme ConnectPubMedGoogle Scholar
  • 55 Thompson KM, Whinton AK, Ferth S, Spriet LL, Burr JF. Ischemic pre-conditioning does not influence maximal sprint acceleration performance. Int J Sports Physiol Perform 2018; 18: 1-16
    PubMedGoogle 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
    Article in Thieme ConnectPubMedGoogle Scholar
  • 57 Tokuno S, Hinokiyama K, Tokuno K, Löwbeer C, Hansson LO, Valen G. Spontaneous ischemic events in the brain and heart adapt the hearts of severely atherosclerotic mice to ischemia. Arterioscler Thromb Vasc Biol 2002; 22: 995-1001
    CrossrefPubMedGoogle Scholar
  • 58 Tomschi F, Bloch W, Grau M. Impact of type of sport, gender and age on red blood cell deformability of elite athletes. Int J Sports Med 2018; 39: 12-20
    Article in Thieme ConnectPubMedGoogle Scholar
  • 59 Wang WZ, Stepheson LL, Fang XH, Khiabani KT, Zamboni WA. Ischemic preconditioning-induced microvascular protection at a distance. J Reconstr Microsurg 2004; 20: 175-181
    Article in Thieme ConnectPubMedGoogle Scholar
  • 60 Yellon DM, Downey JM. Preconditioning the myocardium: From cellular physiology to clinical cardiology. Physiol Rev 2003; 83: 1113-1151
    CrossrefPubMedGoogle Scholar
  • 61 Zinner C, Born DP, Sperlich B. Ischemic preconditioning does not alter performance in multidirectional high-intensity intermittent exercise. Front Physiol 2017; 8: 1029
    CrossrefPubMedGoogle Scholar