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The effect of acute exercise in hypoxia on flow-mediated vasodilation

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Abstract

The purpose of this study was to clarify the effect of acute exercise in hypoxia on flow-mediated vasodilation (FMD). Eight males participated in this study. Two maximal exercise tests were performed using arm cycle ergometry to estimate peak oxygen uptake \( \left( {\dot{V}{\text{O}}_{{ 2 {\text{peak}}}} } \right) \) while breathing normoxic [inspired O2 fraction (FIO2) = 0.21] or hypoxic (FIO2 = 0.12) gas mixtures. Next, subjects performed submaximal exercise at the same relative exercise intensity \( \left( {30\,\% \;\dot{V}{\text{O}}_{{ 2 {\text{peak}}}} } \right) \) in normoxia or hypoxia for 30 min. Before (Pre) and after exercise (Post 5, 30, and 60 min), brachial artery FMD was measured during reactive hyperemia by ultrasound under normoxic conditions. FMD was estimated as the percent (%) rise in the peak diameter from the baseline value at prior occlusion at each FMD measurement (%FMD). The area under the curve for the shear rate stimulus (SRAUC) was calculated in each measurement, and each %FMD value was normalized to SRAUC (normalized FMD). %FMD and normalized FMD decreased significantly (P < 0.05) immediately after exercise in both condition (mean ± SE, FMD, normoxic trial, Pre: 8.85 ± 0.58 %, Post 5: −0.01 ± 1.30 %, hypoxic trial, Pre: 8.84 ± 0.63 %, Post 5: 2.56 ± 0.83 %). At Post 30 and 60, %FMD and normalized FMD returned gradually to pre-exercise levels in both trials (FMD, normoxic trial, Post 30: 1.51 ± 0.68 %, Post 60: 2.99 ± 0.79 %; hypoxic trial, Post 30: 4.57 ± 0.78 %, Post 60: 6.15 ± 1.20 %). %FMD and normalized FMD following hypoxic exercise (at Post 5, 30, and 60) were significantly (P < 0.05) higher than after normoxic exercise. These results suggest that aerobic exercise in hypoxia has a significant impact on endothelial-mediated vasodilation.

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References

  • Babcock M, Shkoukani M, Aboubakr SE, Badr MS (2003) Determinants of long-term facilitation in humans during NREM sleep. J Appl Physiol 94:53–59

    PubMed  Google Scholar 

  • Black MA, Cable NT, Thijssen DH, Green DJ (2008) Importance of measuring the time course of flow-mediated dilatation in humans. Hypertension 51:203–210

    Article  PubMed  CAS  Google Scholar 

  • Blitzer ML, Lee SD, Creager MA (1996) Endothelium-derived nitric oxide mediates hypoxic vasodilation of resistance vessels in humans. Am J Physiol 271:H1182–H1185

    PubMed  CAS  Google Scholar 

  • Borg GAV (1982) Psychophysical bases of perceived exertion. Med Sci Sports Exerc 14:377–381

    PubMed  CAS  Google Scholar 

  • Casey DP, Madery BD, Curry TB, Eisenach JH, Wilkins BW, Joyner MJ (2010) Nitric oxide contributes to the augmented vasodilatation during hypoxic exercise. J Physiol 588:373–385

    Article  PubMed  CAS  Google Scholar 

  • Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D, Vallance P, Vita J, Vogel R (2002) Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 39:257–265

    Article  PubMed  Google Scholar 

  • Cosio-Lima LM, Thompson PD, Reynolds KL, Headley SA, Winter CR, Manos T, Lagasse MA, Todorovich JR, Germain M (2006) The acute effect of aerobic exercise on brachial artery endothelial function in renal transplant recipients. Prev Cardiol 9:211–214

    Article  PubMed  Google Scholar 

  • Dawson EA, Whyte GP, Black MA, Jones H, Hopkins N, Oxborough D, Gaze D, Shave RE, Wilson M, George KP, Green DJ (2008) Changes in vascular and cardiac function after prolonged strenuous exercise in humans. J Appl Physiol 105:1562–1568

    Article  PubMed  Google Scholar 

  • Delp MD, Laughlin MH (1998) Regulation of skeletal muscle perfusion during exercise. Acta Physiol Scand 162:411–419

    Article  PubMed  CAS  Google Scholar 

  • Edmunds NJ, Marshall JM (2001) Vasodilatation, oxygen delivery and oxygen consumption in rat hindlimb during systemic hypoxia: roles of nitric oxide. J Physiol 532:251–259

    Article  PubMed  CAS  Google Scholar 

  • Edwards DG, Schofield RS, Lennon SL, Pierce GL, Nichols WW, Braith RW (2004) Effect of exercise training on endothelial function in men with coronary artery disease. Am J Cardiol 93:617–620

    Article  PubMed  CAS  Google Scholar 

  • Frick M, Rinner A, Mair J, Alber HF, Mittermayr M, Pachinger O, Humpeler E, Schobersberger W, Weidinger F (2006) Transient impairment of flow-mediated vasodilation in patients with metabolic syndrome at moderate altitude (1,700 m). Int J Cardiol 109:82–87

    Article  PubMed  Google Scholar 

  • Gielen S, Schuler G, Hambrecht R (2001) Exercise training in coronary artery disease and coronary vasomotion. Circulation 103:E1–E6

    Article  PubMed  CAS  Google Scholar 

  • Gokce N, Vita JA, Bader DS, Sherman DL, Hunter LM, Holbrook M, O’Malley C, Keaney JF Jr, Balady GJ (2002) Effect of exercise on upper and lower extremity endothelial function in patients with coronary artery disease. Am J Cardiol 90:124–127

    Article  PubMed  Google Scholar 

  • Green D, Cheetham C, Mavaddat L, Watts K, Best M, Taylor R, O’Driscoll G (2002a) Effect of lower limb exercise on forearm vascular function: contribution of nitric oxide. Am J Physiol Heart Circ Physiol 283:H899–H907

    PubMed  CAS  Google Scholar 

  • Green D, Cheetham C, Reed C, Dembo L, O’Driscoll G (2002b) Assessment of brachial artery blood flow across the cardiac cycle: retrograde flows during cycle ergometry. J Appl Physiol 93:361–368

    PubMed  Google Scholar 

  • Hamdy O, Ledbury S, Mullooly C, Jarema C, Porter S, Ovalle K, Moussa A, Caselli A, Caballero AE, Economides PA, Veves A, Horton ES (2003) Lifestyle modification improves endothelial function in obese subjects with the insulin resistance syndrome. Diabetes Care 26:2119–2125

    Article  PubMed  Google Scholar 

  • Harris RA, Padilla J, Rink LD, Wallace JP (2006) Variability of flow-mediated dilation measurements with repetitive reactive hyperemia. Vasc Med 11:1–6

    Article  PubMed  Google Scholar 

  • Harris RA, Padilla J, Hanlon KP, Rink LD, Wallace JP (2007) Reproducibility of the flow-mediated dilation response to acute exercise in overweight men. Ultrasound Med Biol 33:1579–1585

    Article  PubMed  Google Scholar 

  • Harvey PJ, Morris BL, Kubo T, Picton PE, Su WS, Notarius CF, Floras JS (2005) Hemodynamic after-effects of acute dynamic exercise in sedentary normotensive postmenopausal women. J Hypertens 23:285–292

    Article  PubMed  CAS  Google Scholar 

  • Iwamoto E, Katayama K, Oshida Y, Ishida K (2012) Hypoxia augments oscillatory blood flow in brachial artery during leg cycling. Med Sci Sports Exerc 44:1035–1042

    Google Scholar 

  • Katayama K, Amann M (2009) Arterial oxygenation and muscle fatigue. In: Shinohara M (ed) Advances in neuromuscular physiology of motor skills and muscle fatigue. Research Signpost, India, pp 327–350

    Google Scholar 

  • Katayama K, Amann M, Pegelow DF, Jacques AJ, Dempsey JA (2007a) Effect of arterial oxygenation on quadriceps fatigability during isolated muscle exercise. Am J Physiol Regul Integr Comp Physiol 292:R1279–R1286

    Article  PubMed  CAS  Google Scholar 

  • Katayama K, Sato K, Hotta N, Ishida K, Iwasaki K, Miyamura M (2007b) Intermittent hypoxia does not increase exercise ventilation at simulated moderate altitude. Int J Sports Med 28:480–487

    Article  PubMed  CAS  Google Scholar 

  • Katayama K, Yoshitake Y, Watanabe K, Akima H, Ishida K (2010) Muscle deoxygenation during sustained and intermittent isometric exercise in hypoxia. Med Sci Sports Exerc 42:1269–1278

    PubMed  CAS  Google Scholar 

  • Katayama K, Ishida K, Iwamoto E, Iemitsu M, Koike T, Saito M (2011) Hypoxia augments muscle sympathetic neural response to leg cycling. Am J Physiol Regul Integr Comp Physiol 301:R456–R464

    Article  PubMed  CAS  Google Scholar 

  • 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 586:1137–1145

    Article  PubMed  CAS  Google Scholar 

  • Leuenberger UA, Gray K, Herr MD (1999) Adenosine contributes to hypoxia-induced forearm vasodilation in humans. J Appl Physiol 87:2218–2224

    PubMed  CAS  Google Scholar 

  • Leuenberger UA, Johnson D, Loomis J, Gray KS, MacLean DA (2008) Venous but not skeletal muscle interstitial nitric oxide is increased during hypobaric hypoxia. Eur J Appl Physiol 102:457–461

    Article  PubMed  Google Scholar 

  • Maiorana A, O’Driscoll G, Cheetham C, Dembo L, Stanton K, Goodman C, Taylor R, Green D (2001) The effect of combined aerobic and resistance exercise training on vascular function in type 2 diabetes. J Am Coll Cardiol 38:860–866

    Article  PubMed  CAS  Google Scholar 

  • Marshall JM (2000) Adenosine and muscle vasodilatation in acute systemic hypoxia. Acta Physiol Scand 168:561–573

    Article  PubMed  CAS  Google Scholar 

  • Marshall JM (2001) Roles of adenosine and nitric oxide in skeletal muscle in acute and chronic hypoxia. Adv Exp Med Biol 502:349–363

    PubMed  CAS  Google Scholar 

  • Niebauer J, Cooke JP (1996) Cardiovascular effects of exercise: role of endothelial shear stress. J Am Coll Cardiol 28:1652–1660

    Article  PubMed  CAS  Google Scholar 

  • Nishiwaki M, Kawakami R, Saito K, Tamaki H, Takekura H, Ogita F (2011) Vascular adaptations to hypobaric hypoxic training in postmenopausal women. J Physiol Sci 61:83–91

    Article  PubMed  Google Scholar 

  • Padilla J, Harris RA, Fly AD, Rink LD, Wallace JP (2006) The effect of acute exercise on endothelial function following a high-fat meal. Eur J Appl Physiol 98:256–262

    Article  PubMed  CAS  Google Scholar 

  • Padilla J, Harris RA, Wallace JP (2007) Can the measurement of brachial artery flow-mediated dilation be applied to the acute exercise model? Cardiovasc Ultrasound 5:45

    Article  PubMed  Google Scholar 

  • Pyke KE, Tschakovsky ME (2005) The relationship between shear stress and flow-mediated dilatation: implications for the assessment of endothelial function. J Physiol 568:357–369

    Article  PubMed  CAS  Google Scholar 

  • Pyke KE, Tschakovsky ME (2007) Peak vs. total reactive hyperemia: which determines the magnitude of flow-mediated dilation? J Appl Physiol 102:1510–1519

    Article  PubMed  Google Scholar 

  • Pyke KE, Poitras V, Tschakovsky ME (2008) Brachial artery flow-mediated dilation during handgrip exercise: evidence for endothelial transduction of the mean shear stimulus. Am J Physiol Heart Circ Physiol 294:H2669–H2679

    Article  PubMed  CAS  Google Scholar 

  • Ray CJ, Marshall JM (2005) Measurement of nitric oxide release evoked by systemic hypoxia and adenosine from rat skeletal muscle in vivo. J Physiol 568:967–978

    Article  PubMed  CAS  Google Scholar 

  • Reboul C, Tanguy S, Dauzat M, Obert P (2005a) Altitude negates the benefits of aerobic training on the vascular adaptations in rats. Med Sci Sports Exerc 37:979–985

    PubMed  Google Scholar 

  • Reboul C, Tanguy S, Gibault A, Dauzat M, Obert P (2005b) Chronic hypoxia exposure depresses aortic endothelium-dependent vasorelaxation in both sedentary and trained rats: involvement of l-arginine. J Appl Physiol 99:1029–1035

    Article  PubMed  CAS  Google Scholar 

  • Rognmo O, Bjornstad TH, Kahrs C, Tjonna AE, Bye A, Haram PM, Stolen T, Slordahl SA, Wisloff U (2008) Endothelial function in highly endurance-trained men: effects of acute exercise. J Strength Cond Res 22:535–542

    Article  PubMed  Google Scholar 

  • Rowell LB (1986) Cardiovascular adjustments to hypoxemia. In: Rowell LB (ed) Human circulation: regulation during physical stress. Oxford University Press, New York, pp 328–362

    Google Scholar 

  • Seals DR, Johnson DG, Fregosi RF (1991) Hypoxia potentiates exercise-induced sympathetic neural activation in humans. J Appl Physiol 71:1032–1040

    PubMed  CAS  Google Scholar 

  • Sorensen KE, Celermajer DS, Spiegelhalter DJ, Georgakopoulos D, Robinson J, Thomas O, Deanfield JE (1995) Non-invasive measurement of human endothelium dependent arterial responses: accuracy and reproducibility. Br Heart J 74:247–253

    Article  PubMed  CAS  Google Scholar 

  • Tanaka H, Bassett DR Jr, Turner MJ (1996) Exaggerated blood pressure response to maximal exercise in endurance-trained individuals. Am J Hypertens 9:1099–1103

    Article  PubMed  CAS  Google Scholar 

  • Tanaka H, Shimizu S, Ohmori F, Muraoka Y, Kumagai M, Yoshizawa M, Kagaya A (2006) Increases in blood flow and shear stress to nonworking limbs during incremental exercise. Med Sci Sports Exerc 38:81–85

    Article  PubMed  Google Scholar 

  • Thijssen DH, de Groot P, Kooijman M, Smits P, Hopman MT (2006) Sympathetic nervous system contributes to the age-related impairment of flow-mediated dilation of the superficial femoral artery. Am J Physiol Heart Circ Physiol 291:H3122–H3129

    Article  PubMed  CAS  Google Scholar 

  • Thijssen DH, Black MA, Pyke KE, Padilla J, Atkinson G, Harris RA, Parker B, Widlansky ME, Tschakovsky ME, Green DJ (2011) Assessment of flow-mediated dilation in humans: a methodological and physiological guideline. Am J Physiol Heart Circ Physiol 300:H2–H12

    Article  PubMed  CAS  Google Scholar 

  • Thompson PD, Crouse SF, Goodpaster B, Kelley D, Moyna N, Pescatello L (2001) The acute versus the chronic response to exercise. Med Sci Sports Exerc 33:S438–S445 (discussion S452–S433)

    Article  PubMed  CAS  Google Scholar 

  • Tinken TM, Thijssen DH, Black MA, Cable NT, Green DJ (2008) Time course of change in vasodilator function and capacity in response to exercise training in humans. J Physiol 586:5003–5012

    Article  PubMed  CAS  Google Scholar 

  • Tinken TM, Thijssen DH, Hopkins N, Black MA, Dawson EA, Minson CT, Newcomer SC, Laughlin MH, Cable NT, Green DJ (2009) Impact of shear rate modulation on vascular function in humans. Hypertension 54:278–285

    Article  PubMed  CAS  Google Scholar 

  • Tschakovsky ME, Joyner MJ (2008) Nitric oxide and muscle blood flow in exercise. Appl Physiol Nutr Metab 33:151–161

    Article  PubMed  CAS  Google Scholar 

  • Tyldum GA, Schjerve IE, Tjonna AE, Kirkeby-Garstad I, Stolen TO, Richardson RS, Wisloff U (2009) Endothelial dysfunction induced by post-prandial lipemia: complete protection afforded by high-intensity aerobic interval exercise. J Am Coll Cardiol 53:200–206

    Article  PubMed  CAS  Google Scholar 

  • Uehata A, Lieberman EH, Gerhard MD, Anderson TJ, Ganz P, Polak JF, Creager MA, Yeung AC (1997) Noninvasive assessment of endothelium-dependent flow-mediated dilation of the brachial artery. Vasc Med 2:87–92

    PubMed  CAS  Google Scholar 

  • Victor RG, Seals DR, Mark AL (1987) Differential control of heart rate and sympathetic nerve activity during dynamic exercise. Insight from intraneural recordings in humans. J Clin Invest 79:508–516

    Article  PubMed  CAS  Google Scholar 

  • Xie A, Skatrud JB, Puleo DS, Morgan BJ (2001) Exposure to hypoxia produces long-lasting sympathetic activation in humans. J Appl Physiol 91:1555–1562

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported in part by a Grant-in-Aid for Scientific Research from the Japanese Ministry of Education, Science, Sports and Culture (Grant No. 21300239 and 22700649) and from the Meiji Yasuda Life Foundation of Health and Welfare.

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Correspondence to Keisho Katayama.

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Communicated by Massimo Pagani.

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Katayama, K., Fujita, O., Iemitsu, M. et al. The effect of acute exercise in hypoxia on flow-mediated vasodilation. Eur J Appl Physiol 113, 349–357 (2013). https://doi.org/10.1007/s00421-012-2442-5

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