Abstract
Excessive arterial pressure elevation induced by resistance exercise (RE) attenuates peripheral vasodilatory function, but its effect on cerebrovascular function is unknown. We aimed to evaluate the effect of different pressor responses to RE on hypercapnia-induced vasodilation of the internal carotid artery (ICA), an index of cerebrovascular function. To manipulate pressor responses to RE, 15 healthy young adults (11M/4F) performed two RE: high intensity with low repetitions (HL) and low intensity with high repetitions (LH) dynamic knee extension. ICA dilation, induced by 3 min of hypercapnia, was measured before and 10 min after RE using Doppler ultrasound. HL exercise elicited a greater pressor response than LH exercise. In relaxation phases of RE, ICA blood velocity increased in both HL and LH trials. However, ICA shear rate did not significantly increase in either trial (P = 0.06). Consequently, neither exercise altered post-exercise hypercapnia-induced ICA dilation (HL, 3.9 ± 1.9% to 5.1 ± 1.7%; LH, 4.6 ± 1.4% to 4.8 ± 1.8%; P > 0.05 for all). When viewed individually, the changes in ICA shear rate were positively correlated with changes in end-tidal partial pressure of carbon dioxide (PETCO2) (r = 0.46, P < 0.01) than with mean arterial pressure (r = 0.32, P = 0.02). These findings suggest that the effects of RE-induced pressor response on cerebrovascular function may be different from peripheral arteries. An increase in PETCO2 during the relaxation phase may play a more crucial role than elevated pressure in increasing cerebral shear during dynamic RE.
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Abbreviations
- ANCOVA:
-
Analysis of covariance
- ANOVA:
-
Analysis of variance
- BP:
-
Blood pressure
- CO2 :
-
Carbon dioxide
- D base :
-
Baseline diameter
- D peak :
-
Peak diameter
- Ex-ΔSR:
-
Exercise-induced increases in shear rate
- FMD:
-
Flow-mediated dilation
- HL:
-
High intensity with low repetitions
- ICA:
-
Internal carotid artery
- LBNP:
-
Lower-body negative pressure
- LH:
-
Low intensity with high repetitions
- MAP:
-
Mean arterial pressure
- MCAv:
-
Middle cerebral artery blood velocity
- MCAvmean :
-
Time-averaged mean middle cerebral artery blood velocity
- PETCO2 :
-
End-tidal partial pressure of carbon dioxide
- RE:
-
Resistance exercise
- RR:
-
Respiratory rate
- SNA:
-
Sympathetic nerve activity
- SR:
-
Shear rate
- SRAUC :
-
Shear rate area under the curve
- SRbase :
-
Baseline shear rate
- SRpeak :
-
Peak shear rate
- \(\dot{V}\) E :
-
Minute ventilation
- V mean :
-
Time-averaged mean blood velocity
- V T :
-
Tidal volume
- 1RM:
-
One repetition maximum
- η 2 :
-
Eta-squared
- η 2 p :
-
Partial eta-squared
References
Atkinson G, Batterham AM (2013) The percentage flow-mediated dilation index: a large-sample investigation of its appropriateness, potential for bias and causal nexus in vascular medicine. Vasc Med 18:354–365. https://doi.org/10.1177/1358863x13508446
Atkinson G, Batterham AM, Thijssen DH, Green DJ (2013) A new approach to improve the specificity of flow-mediated dilation for indicating endothelial function in cardiovascular research. J Hypertens 31:287–291. https://doi.org/10.1097/HJH.0b013e32835b8164
Atkinson CL, Carter HH, Naylor LH, Dawson EA, Marusic P, Hering D, Schlaich MP, Thijssen DH, Green DJ (2015a) Opposing effects of shear-mediated dilation and myogenic constriction on artery diameter in response to handgrip exercise in humans. J Appl Physiol 119:858–864. https://doi.org/10.1152/japplphysiol.01086.2014
Atkinson CL, Lewis NC, Carter HH, Thijssen DH, Ainslie PN, Green DJ (2015b) Impact of sympathetic nervous system activity on post-exercise flow-mediated dilatation in humans. J Physiol 593:5145–5156. https://doi.org/10.1113/JP270946
Barnes JN, Taylor JL, Kluck BN, Johnson CP, Joyner MJ (2013) Cerebrovascular reactivity is associated with maximal aerobic capacity in healthy older adults. J Appl Physiol 114:1383–1387. https://doi.org/10.1152/japplphysiol.01258.2012
Berdeaux A, Ghaleh B, Dubois-Randé JL, Vigué B, Drieu La Rochelle C, Hittinger L, Giudicelli JF (1994) Role of vascular endothelium in exercise-induced dilation of large epicardial coronary arteries in conscious dogs. Circulation 89:2799–2808. https://doi.org/10.1161/01.cir.89.6.2799
Billinger SA, Arena R, Bernhardt J, Eng JJ, Franklin BA, Johnson CM, MacKay-Lyons M, Macko RF, Mead GE, Roth EJ, Shaughnessy M, Tang A (2014) Physical activity and exercise recommendations for stroke survivors: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 45:2532–2553. https://doi.org/10.1161/str.0000000000000022
Boidin M, Erskine RM, Thijssen DH, Dawson EA (2021) Exercise modality, but not exercise training, alters the acute effect of exercise on endothelial function in healthy men. J Appl Physiol 130:1716–1723. https://doi.org/10.1152/japplphysiol.00004.2021
Brassard P, Tymko MM, Ainslie PN (2017) Sympathetic control of the brain circulation: appreciating the complexities to better understand the controversy. Auton Neurosci 207:37–47. https://doi.org/10.1016/j.autneu.2017.05.003
Buchanan CE, Kadlec AO, Hoch AZ, Gutterman DD, Durand MJ (2017) Hypertension during weight lifting reduces flow-mediated dilation in nonathletes. Med Sci Sports Exerc 49:669–675. https://doi.org/10.1249/mss.0000000000001150
Carr J, Ainslie PN (2020) Shearing the brain. J Appl Physiol 129:599–602. https://doi.org/10.1152/japplphysiol.00658.2020
Carr J, Hoiland RL, Caldwell HG, Coombs GB, Howe CA, Tremblay JC, Green DJ, Ainslie PN (2020) Internal carotid and brachial artery shear-dependent vasodilator function in young healthy humans. J Physiol 598:5333–5350. https://doi.org/10.1113/jp280369
Carter HH, Atkinson CL, Heinonen IH, Haynes A, Robey E, Smith KJ, Ainslie PN, Hoiland RL, Green DJ (2016) Evidence for shear stress-mediated dilation of the internal carotid artery in humans. Hypertension 68:1217–1224. https://doi.org/10.1161/HYPERTENSIONAHA.116.07698
Chesler M (2003) Regulation and modulation of pH in the brain. Physiol Rev 83(4):1183–1221. https://doi.org/10.1152/physrev.00010.2003
Claassen J, Thijssen DHJ, Panerai RB, Faraci FM (2021) Regulation of cerebral blood flow in humans: physiology and clinical implications of autoregulation. Physiol Rev 101:1487–1559. https://doi.org/10.1152/physrev.00022.2020
Dawson EA, Green DJ, Cable NT, Thijssen DH (2013) Effects of acute exercise on flow-mediated dilatation in healthy humans. J Appl Physiol 115:1589–1598. https://doi.org/10.1152/japplphysiol.00450.2013
Dawson EA, Cable NT, Green DJ, Thijssen DH (2018) Do acute effects of exercise on vascular function predict adaptation to training? Eur J Appl Physiol 118:523–530. https://doi.org/10.1007/s00421-017-3724-8
de Oliveira GV, Mendes Cordeiro E, Volino-Souza M, Rezende C, Conte-Junior CA, Silveira Alvares T (2020) Flow-mediated dilation in healthy young individuals is impaired after a single resistance exercise session. Int J Environ Res Public Health 17:5194. https://doi.org/10.3390/ijerph17145194
Dickerman RD, McConathy WJ, Smith GH, East JW, Rudder L (2000) Middle cerebral artery blood flow velocity in elite power athletes during maximal weight-lifting. Neurol Res 22:337–340. https://doi.org/10.1080/01616412.2000.11740679
Edwards MR, Martin DH, Hughson RL (2002) Cerebral hemodynamics and resistance exercise. Med Sci Sports Exerc 34:1207–1211. https://doi.org/10.1097/00005768-200207000-00024
Favre ME, Serrador JM (2019) Sex differences in cerebral autoregulation are unaffected by menstrual cycle phase in young, healthy women. Am J Physiol Heart Circ Physiol 316:920–933. https://doi.org/10.1152/ajpheart.00474.2018
Fernandes IA, Mattos JD, Campos MO, Machado AC, Rocha MP, Rocha NG, Vianna LC, Nobrega AC (2016) Selective alpha1-adrenergic blockade disturbs the regional distribution of cerebral blood flow during static handgrip exercise. Am J Physiol Heart Circ Physiol 310:1541–1548. https://doi.org/10.1152/ajpheart.00125.2016
Forde C, Johnston M, Haberlin C, Breen P, Greenan S, Gissane C, Comyns T, Maher V, Gormley J (2020) Low dose resistance exercise: a pilot study examining effects on blood pressure and augmentation index between intensities. High Blood Press Cardiovasc Prev 27:83–91. https://doi.org/10.1007/s40292-020-00362-5
Garber CE, Blissmer B, Deschenes MR, Franklin BA, Lamonte MJ, Lee IM, Nieman DC, Swain DP, College A, of Sports M, (2011) American College of Sports Medicine position stand. Quantity and quality of exercise for develo** and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc 43:1334–1359. https://doi.org/10.1249/MSS.0b013e318213fefb
Green DJ, Hopman MT, Padilla J, Laughlin MH, Thijssen DH (2017) Vascular adaptation to exercise in humans: role of hemodynamic stimuli. Physiol Rev 97:495–528. https://doi.org/10.1152/physrev.00014.2016
Hardebo JE (1992) Influence of impulse pattern on noradrenaline release from sympathetic nerves in cerebral and some peripheral vessels. Acta Physiol Scand 144:333–339. https://doi.org/10.1111/j.1748-1716.1992.tb09302.x
Hartwich D, Fowler KL, Wynn LJ, Fisher JP (2010) Differential responses to sympathetic stimulation in the cerebral and brachial circulations during rhythmic handgrip exercise in humans. Exp Physiol 95:1089–1097. https://doi.org/10.1113/expphysiol.2010.054387
Hijmering ML, Stroes ESG, Olijhoek J, Hutten BA, Blankestijn PJ, Rabelink TJ (2002) Sympathetic activation markedly reduces endothelium-dependent, flow-mediated vasodilation. J Am Coll Cardiol 39:683–688. https://doi.org/10.1016/s0735-1097(01)01786-7
Hoiland RL, Caldwell HG, Carr J, Howe CA, Stacey BS, Dawkins T, Wakeham DJ, Tremblay JC, Tymko MM, Patrician A, Smith KJ, Sekhon MS, MacLeod DB, Green DJ, Bailey DM, Ainslie PN (2021) Nitric oxide contributes to cerebrovascular shear-mediated dilation but not steady-state cerebrovascular reactivity to carbon dioxide. J Physiol 600:1385–1403. https://doi.org/10.1113/jp282427
Holder SM, Dawson EA, Brislane A, Hisdal J, Green DJ, Thijssen DH (2019) Fluctuation in shear rate, with unaltered mean shear rate, improves brachial artery flow-mediated dilation in healthy, young men. J Appl Physiol 126:1687–1693. https://doi.org/10.1152/japplphysiol.00009.2019
Iwamoto E, Ogoh S (2020) Fluctuating shear during resistance exercise. Exp Physiol 105:2004–2006. https://doi.org/10.1113/ep089174
Iwamoto E, Bock JM, Casey DP (2018a) Blunted shear-mediated dilation of the internal but not common carotid artery in response to lower body negative pressure. J Appl Physiol 124:1326–1332. https://doi.org/10.1152/japplphysiol.01011.2017
Iwamoto E, Bock JM, Casey DP (2018b) Hypercapnia-induced shear-mediated dilation in the internal carotid artery is blunted in healthy older adults. Am J Physiol Heart Circ Physiol 315:1279–1286. https://doi.org/10.1152/ajpheart.00335.2018
Iwamoto E, Hanson BE, Bock JM, Casey DP (2020a) Intermittent hypoxia enhances shear-mediated dilation of the internal carotid artery in young adults. J Appl Physiol 129:603–611. https://doi.org/10.1152/japplphysiol.00274.2020
Iwamoto E, Sakamoto R, Tsuchida W, Yamazaki K, Kamoda T, Neki T, Katayose M, Casey DP (2020b) Effects of menstrual cycle and menopause on internal carotid artery shear-mediated dilation in women. Am J Physiol Heart Circ Physiol 320:679–689. https://doi.org/10.1152/ajpheart.00810.2020
Jurva JW, Phillips SA, Syed AQ, Syed AY, Pitt S, Weaver A, Gutterman DD (2006) The effect of exertional hypertension evoked by weight lifting on vascular endothelial function. J Am Coll Cardiol 48:588–589. https://doi.org/10.1016/j.jacc.2006.05.004
Karlsson WK, Sorensen CG, Kruuse C (2017) l-arginine and l-NMMA for assessing cerebral endothelial dysfunction in ischaemic cerebrovascular disease: a systematic review. Clin Exp Pharmacol Physiol 44:13–20. https://doi.org/10.1111/1440-1681.12679
Kaur J, Vranish JR, Barbosa TC, Washio T, Young BE, Stephens BY, Brothers RM, Ogoh S, Fadel PJ (2018) Regulation of regional cerebral blood flow during graded reflex-mediated sympathetic activation via lower body negative pressure. J Appl Physiol 125:1779–1786. https://doi.org/10.1152/japplphysiol.00623.2018
Koch A, Ivers M, Gehrt A, Schnoor P, Rump A, Rieckert H (2005) Cerebral autoregulation is temporarily disturbed in the early recovery phase after dynamic resistance exercise. Clin Auton Res 15:83–91. https://doi.org/10.1007/s10286-005-0249-8
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. https://doi.org/10.1113/jphysiol.2007.145722
Morishima T, Tsuchiya Y, Iemitsu M, Ochi E (2018) High-intensity resistance exercise with low repetitions maintains endothelial function. Am J Physiol Heart Circ Physiol 315:681–686. https://doi.org/10.1152/ajpheart.00281.2018
Morishima T, Iemitsu M, Ochi E (2019) Short-term cycling restores endothelial dysfunction after resistance exercise. Scand J Med Sci Sports 29:1115–1120. https://doi.org/10.1111/sms.13434
Morishima T, Padilla J, Tsuchiya Y, Ochi E (2020) Maintenance of endothelial function following acute resistance exercise in females is associated with a tempered blood pressure response. J Appl Physiol 129:792–799. https://doi.org/10.1152/japplphysiol.00378.2020
Murrell CJ, Cotter JD, Thomas KN, Lucas SJ, Williams MJ, Ainslie PN (2013) Cerebral blood flow and cerebrovascular reactivity at rest and during sub-maximal exercise: effect of age and 12-week exercise training. Age 35:905–920. https://doi.org/10.1007/s11357-012-9414-x
Nielsen KC, Owman C (1967) Adrenergic innervation of pial arteries related to the circle of Willis in the cat. Brain Res 6:773–776. https://doi.org/10.1016/0006-8993(67)90134-5
Ogoh S (2008) Autonomic control of cerebral circulation: exercise. Med Sci Sports Exerc 40(12):2046–2054. https://doi.org/10.1249/MSS.0b013e318180bc6f
Ogoh S (2019) Interaction between the respiratory system and cerebral blood flow regulation. J Appl Physiol 127:1197–1205. https://doi.org/10.1152/japplphysiol.00057.2019
Ogoh S, Washio T, Suzuki K, Iemitsu M, Hashimoto T, Iwamoto E, Bailey DM (2021) Greater increase in internal carotid artery shear rate during aerobic interval compared to continuous exercise in healthy adult men. Physiol Rep 9:e14705. https://doi.org/10.14814/phy2.14705
Perry BG, Lucas SJE (2021) The acute cardiorespiratory and cerebrovascular response to resistance exercise. Sports Med Open 7:36. https://doi.org/10.1186/s40798-021-00314-w
Phillips SA, Das E, Wang J, Pritchard K, Gutterman DD (2011) Resistance and aerobic exercise protects against acute endothelial impairment induced by a single exposure to hypertension during exertion. J Appl Physiol 110:1013–1020. https://doi.org/10.1152/japplphysiol.00438.2010
Portegies ML, de Bruijn RF, Hofman A, Koudstaal PJ, Ikram MA (2014) Cerebral vasomotor reactivity and risk of mortality: the Rotterdam study. Stroke 45:42–47. https://doi.org/10.1161/strokeaha.113.002348
Rodrigues JCL, Strelko G, Warnert EAH, Burchell AE, Neumann S, Ratcliffe LEK, Harris AD, Chant B, Bowles R, Nightingale AK, Wise RG, Paton JFR, Hart EC (2020) Retrograde blood flow in the internal jugular veins of humans with hypertension may have implications for cerebral arterial blood flow. Eur Radiol 30:3890–3899. https://doi.org/10.1007/s00330-020-06752-6
Rosenberg AJ, Schroeder EC, Grigoriadis G, Wee SO, Bunsawat K, Heffernan KS, Fernhall B, Baynard T (2020) Aging reduces cerebral blood flow regulation following an acute hypertensive stimulus. J Appl Physiol 128:1186–1195. https://doi.org/10.1152/japplphysiol.00137.2019
Sakamoto R, Katayose M, Yamada Y, Neki T, Kamoda T, Tamai K, Yamazaki K, Iwamoto E (2021) High-but not moderate-intensity exercise acutely attenuates hypercapnia-induced vasodilation of the internal carotid artery in young men. Eur J Appl Physiol 121:2471–2485. https://doi.org/10.1007/s00421-021-04721-5
Smith KJ, Hoiland RL, Grove R, McKirdy H, Naylor L, Ainslie PN, Green DJ (2017) Matched increases in cerebral artery shear stress, irrespective of stimulus, induce similar changes in extra-cranial arterial diameter in humans. J Cereb Blood Flow Metab 39:849–858. https://doi.org/10.1177/0271678X17739220
Sugawara J, Brothers RM, Raven PB, Okazaki K, Ogoh S (2013) Effect of systemic α1-adrenergic receptor blockade on central blood pressure response during exercise. J Physiol Sci 63:389–393. https://doi.org/10.1007/s12576-013-0272-9
Suzuki K, Washio T, Tsukamoto S, Kato K, Iwamoto E, Ogoh S (2020) Habitual cigarette smoking attenuates shear-mediated dilation in the brachial artery but not in the carotid artery in young adults. Physiol Rep 8:e14369–e14369. https://doi.org/10.14814/phy2.14369
Thomas KN, Kissling LS, Gibbons TD, Akerman AP, van Rij AM, Cotter JD (2020) The acute effect of resistance exercise on limb blood flow. Exp Physiol 105:2099–2109. https://doi.org/10.1113/ep088743
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. https://doi.org/10.1161/HYPERTENSIONAHA.109.134361
Varady KA, Bhutani S, Church EC, Phillips SA (2010) Adipokine responses to acute resistance exercise in trained and untrained men. Med Sci Sports Exerc 42:456–462. https://doi.org/10.1249/MSS.0b013e3181ba6dd3
Verbree J, Bronzwaer A, van Buchem MA, Daemen M, van Lieshout JJ, van Osch M (2017) Middle cerebral artery diameter changes during rhythmic handgrip exercise in humans. J Cereb Blood Flow Metab 37:2921–2927. https://doi.org/10.1177/0271678x16679419
Warnert EAH, Hart EC, Hall JE, Murphy K, Wise RG (2016) The major cerebral arteries proximal to the Circle of Willis contribute to cerebrovascular resistance in humans. J Cereb Blood Flow Metab 36(8):1384–1395. https://doi.org/10.1177/0271678x15617952
Willie CK, Colino FL, Bailey DM, Tzeng YC, Binsted G, Jones LW, Haykowsky MJ, Bellapart J, Ogoh S, Smith KJ, Smirl JD, Day TA, Lucas SJ, Eller LK, Ainslie PN (2011) Utility of transcranial Doppler ultrasound for the integrative assessment of cerebrovascular function. J Neurosci Methods 196:221–237. https://doi.org/10.1016/j.jneumeth.2011.01.011
Willie CK, Tzeng YC, Fisher JA, Ainslie PN (2014) Integrative regulation of human brain blood flow. J Physiol 592:841–859. https://doi.org/10.1113/jphysiol.2013.268953
Yeboah J, Folsom AR, Burke GL, Johnson C, Polak JF, Post W, Lima JA, Crouse JR, Herrington DM (2009) Predictive value of brachial flow-mediated dilation for incident cardiovascular events in a population-based study: the multi-ethnic study of atherosclerosis. Circulation 120:502–509. https://doi.org/10.1161/CIRCULATIONAHA.109.864801
Acknowledgements
The authors would like to thank Ryota Tsukahara for the technical assistance. We appreciate the commitment of all participants of this study.
Funding
R.S. was supported by a Grant-in-Aid for Scientific Research (Grant No. 21J22042) from the Japanese Ministry of Education, Culture, Sports, Science and Technology. E.I. was supported by a Grant-in-Aid for Scientific Research (Grant No. 20K11186) from the Japanese Ministry of Education, Culture, Sports, Science and Technology.
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RS, KS and EI were the principal investigators and, in conjunction with SO and MK, were responsible for the conception and design of the research. RS, KS, TK, TN and EI performed the experiments. RS and KS analysed the data. RS, SO and EI wrote the original manuscript and interpreted the results of the experiments. RS prepared the figures. All authors edited and revised the manuscript. All authors approved the final version of manuscript.
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Sakamoto, R., Sato, K., Ogoh, S. et al. Dynamic resistance exercise-induced pressor response does not alter hypercapnia-induced cerebral vasodilation in young adults. Eur J Appl Physiol 123, 781–796 (2023). https://doi.org/10.1007/s00421-022-05096-x
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DOI: https://doi.org/10.1007/s00421-022-05096-x