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Open Access 01-03-2022 | Original Article

Aortic haemodynamics: the effects of habitual endurance exercise, age and muscle sympathetic vasomotor outflow in healthy men

Authors: Denis J. Wakeham, Tony G. Dawkins, Rachel N. Lord, Jack S. Talbot, Freya M. Lodge, Bryony A. Curry, Lydia L. Simpson, Christopher J. A. Pugh, Robert E. Shave, Jonathan P. Moore

Published in: European Journal of Applied Physiology | Issue 3/2022

Abstract

Purpose

We determined the effect of habitual endurance exercise and age on aortic pulse wave velocity (aPWV), augmentation pressure (AP) and systolic blood pressure (aSBP), with statistical adjustments of aPWV and AP for heart rate and aortic mean arterial pressure, when appropriate. Furthermore, we assessed whether muscle sympathetic nerve activity (MSNA) correlates with AP in young and middle-aged men.

Methods

Aortic PWV, AP, aortic blood pressure (applanation tonometry; SphygmoCor) and MSNA (peroneal microneurography) were recorded in 46 normotensive men who were either young or middle-aged and endurance-trained runners or recreationally active nonrunners (10 nonrunners and 13 runners within each age-group). Between-group differences and relationships between variables were assessed via ANOVA/ANCOVA and Pearson product-moment correlation coefficients, respectively.

Results

Adjusted aPWV and adjusted AP were similar between runners and nonrunners in both age groups (all, P > 0.05), but higher with age (all, P < 0.001), with a greater effect size for the age-related difference in AP in runners (Hedges’ g, 3.6 vs 2.6). aSBP was lower in young (P = 0.009; g = 2.6), but not middle-aged (P = 0.341; g = 1.1), runners compared to nonrunners. MSNA burst frequency did not correlate with AP in either age group (young: r = 0.00, P = 0.994; middle-aged: r = − 0.11, P = 0.604).

Conclusion

There is an age-dependent effect of habitual exercise on aortic haemodynamics, with lower aSBP in young runners compared to nonrunners only. Statistical adjustment of aPWV and AP markedly influenced the outcomes of this study, highlighting the importance of performing these analyses. Further, peripheral sympathetic vasomotor outflow and AP were not correlated in young or middle-aged normotensive men.

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(6):354–365. https://doi.org/10.1177/1358863X13508446CrossRefPubMed

Bjarnegard N, Lanne T, Cinthio M, Ekstrand J, Hedman K, Nylander E, Henriksson J (2018) Vascular characteristics in young women-Effect of extensive endurance training or a sedentary lifestyle. Acta Physiol (oxf) 223(2):e13041. https://doi.org/10.1111/apha.13041CrossRef

Casey DP, Curry TB, Joyner MJ, Charkoudian N, Hart EC (2011) Relationship between muscle sympathetic nerve activity and aortic wave reflection characteristics in young men and women. Hypertension 57(3):421–427. https://doi.org/10.1161/HYPERTENSIONAHA.110.164517CrossRefPubMed

Charkoudian N, Wallin BG (2014) Sympathetic neural activity to the cardiovascular system: integrator of systemic physiology and interindividual characteristics. Compr Physiol 4(2):825–850. https://doi.org/10.1002/cphy.c130038CrossRefPubMed

Cohen J (1992) A power primer. Psychol Bull 112(1):155–159. https://doi.org/10.1037//0033-2909.112.1.155CrossRef

Dampney RAL (2017) Resetting of the Baroreflex Control of Sympathetic Vasomotor Activity during Natural Behaviors: Description and Conceptual Model of Central Mechanisms. Front Neurosci 11:461. https://doi.org/10.3389/fnins.2017.00461CrossRefPubMedPubMedCentral

Davies JE, Baksi J, Francis DP, Hadjiloizou N, Whinnett ZI, Manisty CH, Aguado-Sierra J, Foale RA, Malik IS, Tyberg JV, Parker KH, Mayet J, Hughes AD (2010) The arterial reservoir pressure increases with aging and is the major determinant of the aortic augmentation index. Am J Physiol Heart Circ Physiol 298(2):H580-586. https://doi.org/10.1152/ajpheart.00875.2009CrossRefPubMed

Denham J, Brown NJ, Tomaszewski M, Williams B, O’Brien BJ, Charchar FJ (2016) Aortic augmentation index in endurance athletes: a role for cardiorespiratory fitness. Eur J Appl Physiol 116(8):1537–1544. https://doi.org/10.1007/s00421-016-3407-xCrossRefPubMed

Edwards DG, Lang JT (2005) Augmentation index and systolic load are lower in competitive endurance athletes. Am J Hypertens 18(5 Pt 1):679–683. https://doi.org/10.1016/j.amjhyper.2004.11.028CrossRefPubMed

Fagius J, Wallin BG (1993) Long-term variability and reproducibility of resting human muscle nerve sympathetic activity at rest, as reassessed after a decade. Clin Auton Res 3(3):201–205. https://doi.org/10.1007/bf01826234CrossRefPubMed

Fonkoue IT, Carter JR (2015) Sympathetic neural reactivity to mental stress in humans: test-retest reproducibility. Am J Physiol Regul Integr Comp Physiol 309(11):R1380-1386. https://doi.org/10.1152/ajpregu.00344.2015CrossRefPubMedPubMedCentral

Gates PE, Tanaka H, Graves J, Seals DR (2003) Left ventricular structure and diastolic function with human ageing. Relation to habitual exercise and arterial stiffness. Eur Heart J 24(24):2213–2220. https://doi.org/10.1016/j.ehj.2003.09.026CrossRefPubMed

Grassi G, Bolla G, Seravalle G, Turri C, Lanfranchi A, Mancia G (1997) Comparison between reproducibility and sensitivity of muscle sympathetic nerve traffic and plasma noradrenaline in man. Clin Sci (lond) 92(3):285–289. https://doi.org/10.1042/cs0920285CrossRef

Hart EC, Charkoudian N, Joyner MJ, Barnes JN, Curry TB, Casey DP (2013) Relationship between sympathetic nerve activity and aortic wave reflection characteristics in postmenopausal women. Menopause 20(9):967–972. https://doi.org/10.1097/GME.0b013e3182843b59CrossRefPubMedPubMedCentral

Holwerda SW, Luehrs RE, DuBose L, Collins MT, Wooldridge NA, Stroud AK, Fadel PJ, Abboud FM, Pierce GL (2019) Elevated muscle sympathetic nerve activity contributes to central artery stiffness in young and middle-age/older adults. Hypertension 73(5):1025–1035. https://doi.org/10.1161/HYPERTENSIONAHA.118.12462CrossRefPubMed

Hughes AD, Park C, Davies J, Francis D, Mc GTSA, Mayet J, Parker KH (2013) Limitations of augmentation index in the assessment of wave reflection in normotensive healthy individuals. PLoS ONE 8(3):e59371. https://doi.org/10.1371/journal.pone.0059371CrossRefPubMedPubMedCentral

Huybrechts SA, Devos DG, Vermeersch SJ, Mahieu D, Achten E, de Backer TL, Segers P, van Bortel LM (2011) Carotid to femoral pulse wave velocity: a comparison of real travelled aortic path lengths determined by MRI and superficial measurements. J Hypertens 29(8):1577–1582. https://doi.org/10.1097/HJH.0b013e3283487841CrossRefPubMed

Katona PG, McLean M, Dighton DH, Guz A (1982) Sympathetic and parasympathetic cardiac control in athletes and nonathletes at rest. J Appl Physiol Respir Environ Exerc Physiol 52(6):1652–1657. https://doi.org/10.1152/jappl.1982.52.6.1652CrossRefPubMed

Kimmerly DS, O’Leary DD, Shoemaker JK (2004) Test-retest repeatability of muscle sympathetic nerve activity: influence of data analysis and head-up tilt. Auton Neurosci 114(1–2):61–71. https://doi.org/10.1016/j.autneu.2004.06.005CrossRefPubMed

Knez WL, Sharman JE, Jenkins DG, Coombes JS (2008) Central hemodynamics in ultra-endurance athletes. J Sci Med Sport 11(4):390–395. https://doi.org/10.1016/j.jsams.2006.11.005CrossRefPubMed

Lamarche F, Agharazii M, Madore F, Goupil R (2020) Prediction of cardiovascular events by type I central systolic blood pressure: a prospective study. Hypertension. https://doi.org/10.1161/HYPERTENSIONAHA.120.16163CrossRefPubMed

Lord RN, Wakeham DJ, Pugh CJA, Simpson LL, Talbot JS, Lodge FM, Curry BA, Dawkins TG, Shave RE, Moore JP (2020) The influence of barosensory vessel mechanics on the vascular sympathetic baroreflex: insights into aging and blood pressure homeostasis. Am J Physiol Heart Circ Physiol 319(2):H370–H376. https://doi.org/10.1152/ajpheart.00265.2020CrossRefPubMed

Matsukawa T, Sugiyama Y, Watanabe T, Kobayashi F, Mano T (1998) Gender difference in age-related changes in muscle sympathetic nerve activity in healthy subjects. Am J Physiol 275(5 Pt 2):R1600-1604PubMed

McDonnell BJ, Maki-Petaja KM, Munnery M, Yasmin WIB, Cockcroft JR, McEniery CM (2013) Habitual exercise and blood pressure: age dependency and underlying mechanisms. Am J Hypertens 26(3):334–341. https://doi.org/10.1093/ajh/hps055CrossRefPubMed

McEniery CM, Yasmin HIR, Qasem A, Wilkinson IB, Cockcroft JR, Investigators A (2005) Normal vascular aging: differential effects on wave reflection and aortic pulse wave velocity: the Anglo-Cardiff Collaborative Trial (ACCT). J Am Coll Cardiol 46(9):1753–1760. https://doi.org/10.1016/j.jacc.2005.07.037CrossRefPubMed

Millar PJ, Notarius CF, Haruki N, Floras JS (2019) Heart failure-specific relationship between muscle sympathetic nerve activity and aortic wave reflection. J Card Fail 25(5):404–408. https://doi.org/10.1016/j.cardfail.2019.03.005CrossRefPubMed

Mitchell GF (2014) Arterial stiffness and hypertension: chicken or egg? Hypertension 64(2):210–214. https://doi.org/10.1161/HYPERTENSIONAHA.114.03449CrossRefPubMed

Mynard JP, Kondiboyina A, Kowalski R, Cheung MMH, Smolich JJ (2020) Measurement, analysis and interpretation of pressure/flow waves in blood vessels. Front Physiol 11:1085. https://doi.org/10.3389/fphys.2020.01085CrossRefPubMedPubMedCentral

Namasivayam M, Adji A, O’Rourke MF (2010) Aortic augmentation index and aging: mathematical resolution of a physiological dilemma? Hypertension 56(1):e9-10. https://doi.org/10.1161/HYPERTENSIONAHA.110.153742CrossRefPubMed

Nardone M, Incognito AV, Millar PJ (2018) Evidence for pressure-independent sympathetic modulation of central pulse wave velocity. J Am Heart Assoc. https://doi.org/10.1161/JAHA.117.007971CrossRefPubMedPubMedCentral

Niiranen TJ, Kalesan B, Larson MG, Hamburg NM, Benjamin EJ, Mitchell GF, Vasan RS (2017) Aortic-Brachial Arterial Stiffness Gradient and Cardiovascular Risk in the Community: The Framingham Heart Study. Hypertension 69(6):1022–1028. https://doi.org/10.1161/HYPERTENSIONAHA.116.08917CrossRefPubMed

Notay K, Seed JD, Incognito AV, Doherty CJ, Nardone M, Burns MJ, Millar PJ (2016) Validity and reliability of measuring resting muscle sympathetic nerve activity using short sampling durations in healthy humans. J Appl Physiol (1985) 121(5):1065–1073. https://doi.org/10.1152/japplphysiol.00736.2016CrossRef

Nowak KL, Rossman MJ, Chonchol M, Seals DR (2018) Strategies for achieving healthy vascular aging. Hypertension 71(3):389–402. https://doi.org/10.1161/HYPERTENSIONAHA.117.10439CrossRefPubMed

Officers' UCM (2019) Physical Activity Guidelines. https://www.gov.uk/government/publications/physical-activity-guidelines-uk-chief-medical-officers-report. Accessed 07 May 2020

O’Rourke MF, Mancia G (1999) Arterial stiffness. J Hypertens 17(1):1–4. https://doi.org/10.1097/00004872-199917010-00001CrossRefPubMed

Otsuki T, Maeda S, Iemitsu M, Saito Y, Tanimura Y, Ajisaka R, Miyauchi T (2007a) Relationship between arterial stiffness and athletic training programs in young adult men. Am J Hypertens 20(9):967–973. https://doi.org/10.1016/j.amjhyper.2007.05.001CrossRefPubMed

Otsuki T, Maeda S, Iemitsu M, Saito Y, Tanimura Y, Ajisaka R, Miyauchi T (2007b) Vascular endothelium-derived factors and arterial stiffness in strength- and endurance-trained men. Am J Physiol Heart Circ Physiol 292(2):H786-791. https://doi.org/10.1152/ajpheart.00678.2006CrossRefPubMed

Parry-Williams G, Sharma S (2020) The effects of endurance exercise on the heart: panacea or poison? Nat Rev Cardiol. https://doi.org/10.1038/s41569-020-0354-3CrossRefPubMed

Pauca AL, O’Rourke MF, Kon ND (2001) Prospective evaluation of a method for estimating ascending aortic pressure from the radial artery pressure waveform. Hypertension 38(4):932–937CrossRef

Pierce GL, Casey DP, Fiedorowicz JG, Seals DR, Curry TB, Barnes JN, Wilson DR, Stauss HM (2013) Aortic pulse wave velocity and reflecting distance estimation from peripheral waveforms in humans: detection of age- and exercise training-related differences. Am J Physiol Heart Circ Physiol 305(1):H135-142. https://doi.org/10.1152/ajpheart.00916.2012CrossRefPubMedPubMedCentral

Pierce GL, Harris SA, Seals DR, Casey DP, Barlow PB, Stauss HM (2016) Estimated aortic stiffness is independently associated with cardiac baroreflex sensitivity in humans: role of ageing and habitual endurance exercise. J Hum Hypertens 30(9):513–520. https://doi.org/10.1038/jhh.2016.3CrossRefPubMedPubMedCentral

Rietjens GJ, Kuipers H, Kester AD, Keizer HA (2001) Validation of a computerized metabolic measurement system (Oxycon-Pro) during low and high intensity exercise. Int J Sports Med 22(4):291–294. https://doi.org/10.1055/s-2001-14342CrossRefPubMed

Rossman MJ, LaRocca TJ, Martens CR, Seals DR (2018) Healthy lifestyle-based approaches for successful vascular aging. J Appl Physiol (1985) 125(6):1888–1900. https://doi.org/10.1152/japplphysiol.00521.2018CrossRef

Seals DR, Brunt VE, Rossman MJ (2018) Keynote lecture: strategies for optimal cardiovascular aging. Am J Physiol Heart Circ Physiol 315(2):H183–H188. https://doi.org/10.1152/ajpheart.00734.2017CrossRefPubMedPubMedCentral

Seals DR, Nagy EE, Moreau KL (2019) Aerobic exercise training and vascular function with ageing in healthy men and women. J Physiol 597(19):4901–4914. https://doi.org/10.1113/JP277764CrossRefPubMed

Shibata S, Fujimoto N, Hastings JL, Carrick-Ranson G, Bhella PS, Hearon CM Jr, Levine BD (2018) The effect of lifelong exercise frequency on arterial stiffness. J Physiol 596(14):2783–2795. https://doi.org/10.1113/JP275301CrossRefPubMedPubMedCentral

Shoemaker JK, Badrov MB, Al-Khazraji BK, Jackson DN (2015) Neural control of vascular function in skeletal muscle. Compr Physiol 6(1):303–329. https://doi.org/10.1002/cphy.c150004CrossRefPubMed

Smith MM, Buffington CA, Hamlin RL, Devor ST (2015) Relationship between muscle sympathetic nerve activity and aortic wave reflection characteristics in aerobic- and resistance-trained subjects. Eur J Appl Physiol 115(12):2609–2619. https://doi.org/10.1007/s00421-015-3230-9CrossRefPubMed

Stamatelopoulos KS, Kalpakos D, Protogerou AD, Papamichael CM, Ikonomidis I, Tsitsirikos M, Revela I, Papaioannou TG, Lekakis JP (2006) The combined effect of augmentation index and carotid intima-media thickness on cardiovascular risk in young and middle-aged men without cardiovascular disease. J Hum Hypertens 20(4):273–279. https://doi.org/10.1038/sj.jhh.1001978CrossRefPubMed

Stoner L, Faulkner J, Lowe A, Lambrick DM, Young JM, Love R, Rowlands DS (2014) Should the augmentation index be normalized to heart rate? J Atheroscler Thromb 21(1):11–16. https://doi.org/10.5551/jat.20008CrossRefPubMed

Swierblewska E, Hering D, Kara T, Kunicka K, Kruszewski P, Bieniaszewski L, Boutouyrie P, Somers VK, Narkiewicz K (2010) An independent relationship between muscle sympathetic nerve activity and pulse wave velocity in normal humans. J Hypertens 28(5):979–984. https://doi.org/10.1097/hjh.0b013e328336ed9aCrossRefPubMed

Talbot JS, Lord RN, Wakeham DJ, Dawkins TG, Curry BA, Brown M, Lodge FM, Pugh CJA (2020) The influence of habitual endurance exercise on carotid artery strain and strain rate in young and middle-aged men. Exp Physiol. https://doi.org/10.1113/EP088384CrossRefPubMed

Tan I, Spronck B, Kiat H, Barin E, Reesink KD, Delhaas T, Avolio AP, Butlin M (2016) Heart rate dependency of large artery stiffness. Hypertension 68(1):236–242. https://doi.org/10.1161/HYPERTENSIONAHA.116.07462CrossRefPubMed

Tanaka H (2019) Antiaging effects of aerobic exercise on systemic arteries. Hypertension. https://doi.org/10.1161/HYPERTENSIONAHA.119.13179CrossRefPubMed

Tanaka H, DeSouza CA, Seals DR (1998) Absence of age-related increase in central arterial stiffness in physically active women. Arterioscler Thromb Vasc Biol 18(1):127–132. https://doi.org/10.1161/01.atv.18.1.127CrossRefPubMed

Tarumi T, Gonzales MM, Fallow B, Nualnim N, Pyron M, Tanaka H, Haley AP (2013) Central artery stiffness, neuropsychological function, and cerebral perfusion in sedentary and endurance-trained middle-aged adults. J Hypertens 31(12):2400–2409. https://doi.org/10.1097/HJH.0b013e328364deccCrossRefPubMed

Tarumi T, Yamabe T, Fukuie M, Kimura R, Zhu DC, Ohyama-Byun K, Maeda S, Sugawara J (2021) Proximal aortic compliance in young male endurance athletes: an MRI Study. Med Sci Sports Exerc 53(3):543–550. https://doi.org/10.1249/MSS.0000000000002508CrossRefPubMed

Townsend RR, Wilkinson IB, Schiffrin EL, Avolio AP, Chirinos JA, Cockcroft JR, Heffernan KS, Lakatta EG, McEniery CM, Mitchell GF, Najjar SS, Nichols WW, Urbina EM, Weber T, American Heart Association Council on H (2015) Recommendations for improving and standardizing vascular research on arterial stiffness: a scientific statement from the American Heart Association. Hypertension 66(3):698–722. https://doi.org/10.1161/HYP.0000000000000033CrossRefPubMed

Vaitkevicius PV, Fleg JL, Engel JH, O’Connor FC, Wright JG, Lakatta LE, Yin FC, Lakatta EG (1993) Effects of age and aerobic capacity on arterial stiffness in healthy adults. Circulation 88(4 Pt 1):1456–1462. https://doi.org/10.1161/01.cir.88.4.1456CrossRefPubMed

Van Bortel LM, Laurent S, Boutouyrie P, Chowienczyk P, Cruickshank JK, De Backer T, Filipovsky J, Huybrechts S, Mattace-Raso FU, Protogerou AD, Schillaci G, Segers P, Vermeersch S, Weber T, Artery S, European Society of Hypertension Working Group on Vascular S, Function, European Network for Noninvasive Investigation of Large A (2012) Expert consensus document on the measurement of aortic stiffness in daily practice using carotid-femoral pulse wave velocity. J Hypertens 30(3):445–448. https://doi.org/10.1097/HJH.0b013e32834fa8b0CrossRef

Van Bortel LM, Segers P, De Backer T (2020) Misconceptions about arterial stiffness may lead to erroneous conclusions. Am J Hypertens 33(5):402–404. https://doi.org/10.1093/ajh/hpaa017CrossRefPubMed

Vlachopoulos C, Aznaouridis K, O’Rourke MF, Safar ME, Baou K, Stefanadis C (2010) Prediction of cardiovascular events and all-cause mortality with central haemodynamics: a systematic review and meta-analysis. Eur Heart J 31(15):1865–1871. https://doi.org/10.1093/eurheartj/ehq024CrossRefPubMed

Wakeham DJ, Lord RN, Talbot JS, Lodge FM, Curry BA, Dawkins TG, Simpson LL, Shave RE, Pugh CJA, Moore JP (2019) Upward resetting of the vascular sympathetic baroreflex in middle-aged male runners. Am J Physiol Heart Circ Physiol 317(1):H181–H189. https://doi.org/10.1152/ajpheart.00106.2019CrossRefPubMed

Wang KL, Cheng HM, Sung SH, Chuang SY, Li CH, Spurgeon HA, Ting CT, Najjar SS, Lakatta EG, Yin FC, Chou P, Chen CH (2010) Wave reflection and arterial stiffness in the prediction of 15-year all-cause and cardiovascular mortalities: a community-based study. Hypertension 55(3):799–805. https://doi.org/10.1161/HYPERTENSIONAHA.109.139964CrossRefPubMed

Wilkinson IB, MacCallum H, Flint L, Cockcroft JR, Newby DE, Webb DJ (2000) The influence of heart rate on augmentation index and central arterial pressure in humans. J Physiol 525(Pt 1):263–270. https://doi.org/10.1111/j.1469-7793.2000.t01-1-00263.xCrossRefPubMedPubMedCentral

Wilkinson IB, Mohammad NH, Tyrrell S, Hall IR, Webb DJ, Paul VE, Levy T, Cockcroft JR (2002) Heart rate dependency of pulse pressure amplification and arterial stiffness. Am J Hypertens 15(1 Pt 1):24–30. https://doi.org/10.1016/s0895-7061(01)02252-xCrossRefPubMed

Yan H, Ranadive SM, Heffernan KS, Lane AD, Kappus RM, Cook MD, Wu PT, Sun P, Harvey IS, Woods JA, Wilund KR, Fernhall B (2014) Hemodynamic and arterial stiffness differences between African-Americans and Caucasians after maximal exercise. Am J Physiol Heart Circ Physiol 306(1):H60-68. https://doi.org/10.1152/ajpheart.00710.2013CrossRefPubMed

Title: Aortic haemodynamics: the effects of habitual endurance exercise, age and muscle sympathetic vasomotor outflow in healthy men
Authors: Denis J. Wakeham
Tony G. Dawkins
Rachel N. Lord
Jack S. Talbot
Freya M. Lodge
Bryony A. Curry
Lydia L. Simpson
Christopher J. A. Pugh
Robert E. Shave
Jonathan P. Moore
Publication date: 01-03-2022
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Applied Physiology / Issue 3/2022
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI: https://doi.org/10.1007/s00421-021-04883-2

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Aortic haemodynamics: the effects of habitual endurance exercise, age and muscle sympathetic vasomotor outflow in healthy men

Abstract

Purpose

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

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