Abstract
Purpose
The purpose of the present study was to examine the effect of repeated, single leg heating on lower limb endothelial function.
Methods
Macrovascular function was assessed with superficial femoral artery (SFA) reactive hyperemia flow-mediated dilation (RH-FMD) and sustained stimulus FMD (SS-FMD). Calf microvascular function was assessed as the peak and area under the curve of SFA reactive hyperemia (RH). Participants (n = 13 females, 23 ± 2 yrs) had one leg randomized to the single leg heating intervention (EXP; other leg: control (CON)). The EXP leg underwent 8 weeks of single leg heating via immersion in 42.5 ℃ water for five 35-min sessions/week. At weeks 0, 2, 4, 6, and 8, SFA RH-FMD, SS-FMD (shear stress increased via plantar flexion exercise), and SFA RH flow were measured.
Results
None of the variables changed with repeated, single leg heating (interaction week*limb RH-FMD: p = 0.076; SS-FMD: p = 0.958; RH flow p = 0.955). Covariation for the shear stress stimulus did not alter the FMD results.
Conclusion
Eight weeks of single leg heating did not change SFA endothelial or calf microvascular function. These results are in contrast with previous findings that limb heating improves upper limb endothelial function.
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Data availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Code availability
Not applicable.
Abbreviations
- AUC:
-
Area under the curve
- BP:
-
Blood pressure
- DBP:
-
Diastolic blood pressure
- CON:
-
Control (non-heated) limb
- EXP:
-
Experimental (heated limb)
- FMD:
-
Flow-mediated dilation
- MAP:
-
Mean arterial pressure
- PA:
-
Physical activity
- RH:
-
Reactive hyperemia
- RH-FMD:
-
Reactive hyperemia flow-mediated dilation
- SFA:
-
Superficial femoral artery
- SS-FMD:
-
Sustained shear stress flow-mediated dilation
- SBP:
-
Systolic blood pressure
References
Adkisson EJ, Casey DP, Beck DT, Gurovich AN, Martin JS, Braith RW (2010) Central, peripheral and resistance arterial reactivity: fluctuates during the phases of the menstrual cycle. Exp Biol Med 235:111–118. https://doi.org/10.1258/ebm.2009.009186
Anderson TJ, Charbonneau F, Title LM, Buithieu J, Rose MS, Conradson H et al (2011) Microvascular function predicts cardiovascular events in primary prevention: long-term results from the firefighters and their endothelium (fate) study. Circulation 123:163–169. https://doi.org/10.1161/CIRCULATIONAHA.110.953653
Bailey TG, Cable NT, Miller GD, Sprung VS, Low DA, Jones H (2016) Repeated warm water immersion induces similar cerebrovascular adaptations to 8 weeks of moderate-intensity exercise training in females. Int J Sports Med 37:757–765. https://doi.org/10.1055/s-0042-106899
Beck DT, Martin JS, Casey DP, Braith RW (2014) Exercise training improves endothelial function in resistance arteries of young prehypertensives. J Hum Hypertens 28:303–309. https://doi.org/10.1038/jhh.2013.109
Beery AK, Zucker I (2011) Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev 35:565–572. https://doi.org/10.1016/j.neubiorev.2010.07.002
Birk GK, Dawson EA, Atkinson C, Haynes A, Cable NT, Thijssen DHJ et al (2012) Brachial artery adaptation to lower limb exercise training: role of shear stress. J Appl Physiol 112:1653–1658. https://doi.org/10.1152/japplphysiol.01489.2011
Brett SE, Ritter JM, Chowienczyk PJ (2000) Diastolic blood pressure changes during exercise positively correlate with serum cholesterol and insulin resistance. Circulation 101:611–615. https://doi.org/10.1161/01.CIR.101.6.611
Brunt VE, Eymann TM, Francisco MA, Howard MJ, Minson CT (2016a) Passive heat therapy improves cutaneous microvascular function in sedentary humans via improved nitric oxide-dependent dilation. J Appl Physiol 121:716–723. https://doi.org/10.1152/japplphysiol.00424.2016
Brunt VE, Howard MJ, Francisco MA, Ely BR, Minson CT (2016b) Passive heat therapy improves endothelial function, arterial stiffness and blood pressure in sedentary humans. J Physiol 594:5329–5342. https://doi.org/10.1113/jp272453
Carter H, Spence A, Atkinson C, Pugh CJ, Cable T, Thijssen D et al (2014a) Distinct impacts of blood flow and temperature on cutaneous microvascular adaptation. Med Sci Sports Exerc 46:2113–2121. https://doi.org/10.1249/MSS.0000000000000349
Carter HH, Spence AL, Atkinson CL, Pugh CJA, Naylor LH, Green DJ (2014b) Repeated core temperature elevation induces conduit artery adaptation in humans. Eur J Appl Physiol 114:859–865. https://doi.org/10.1007/s00421-013-2817-2
Cheng JL, MacDonald MJ (2019) Effect of heat stress on vascular outcomes in humans. J Appl Physiol 126:771–781. https://doi.org/10.1152/japplphysiol.00682.2018
Coombs GB, Barak OF, Phillips AA, Mijacika T, Sarafis ZK, Lee AHX et al (2019) Acute heat stress reduces biomarkers of endothelial activation but not macro- or microvascular dysfunction in cervical spinal cord injury. Am J Physiol Heart Circ Physiol 316:H722–H733. https://doi.org/10.1152/ajpheart.00693.2018
Dengel DR, Hagberg JM, Pratley RE, Rogus EM, Goldberg AP (1998) Improvements in blood pressure, glucose metabolism, and lipoprotein lipids after aerobic exercise plus weight loss in obese, hypertensive middle-aged men. Metabolism 47:1075–1082. https://doi.org/10.1016/S0026-0495(98)90281-5
D’Urzo KA, King TJ, Williams JS, Silvester MD, Pyke KE (2018) The impact of menstrual phase on brachial artery flow-mediated dilatation during handgrip exercise in healthy premenopausal women. Exp Physiol 103:291–302. https://doi.org/10.1113/EP086311
Findlay BB, Gupta P, Szijgyarto IC, Pyke KE (2013) Impaired brachial artery flow-mediated vasodilation in response to handgrip exercise-induced increases in shear stress in young smokers. Vasc Med 18:63–71. https://doi.org/10.1177/1358863x13480259
Freedson PS, Melanson E, Sirard J (1998) Calibration of the computer science and applications, inc. Accelerometer. Med Sci Sports Exerc 30:777–781. https://doi.org/10.1097/00005768-199805000-00021
Gaenzer H, Neumayr G, Marschang P, Sturm W, Kirchmair R, Patsch JR (2001) Flow-mediated vasodilation of the femoral and brachial artery induced by exercise in healthy nonsmoking and smoking men. J Am Coll Cardiol 38:1313. https://doi.org/10.1016/S0735-1097(01)01575-3
Gnasso A, Carallo C, Irace C, De Franceschi MS, Mattioli PL, Motti C et al (2001) Association between wall shear stress and flow-mediated vasodilation in healthy men. Atherosclerosis 156:171–176. https://doi.org/10.1016/S0021-9150(00)00617-1
Harris RA, Tedjasaputra V, Zhao J, Richardson RS (2012) Premenopausal women exhibit an inherent protection of endothelial function following a high-fat meal. Reprod Sci 19:221–228. https://doi.org/10.1177/1933719111418125
Howden EJ, Perhonen M, Peshock RM, Zhang R, Arbab-Zadeh A, Adams-Huet B et al (1985) (2015) Females have a blunted cardiovascular response to one year of intensive supervised endurance training. J Appl Physiol 119:37–46. https://doi.org/10.1152/japplphysiol.00092.2015
Huang AL, Silver AE, Shvenke E, Schopfer DW, Jahangir E, Titas MA et al (2007) Predictive value of reactive hyperemia for cardiovascular events in patients with peripheral arterial disease undergoing vascular surgery. Arterioscler Thromb Vasc Biol 27:2113–2119. https://doi.org/10.1161/ATVBAHA.107.147322
Jazuli F, Pyke KE (2011) The impact of baseline artery diameter on flow-mediated vasodilation: a comparison of brachial and radial artery responses to matched levels of shear stress. Am J Physiol Heart Circ Physiol. https://doi.org/10.1152/ajpheart.00487.2011
Ketel IJ, Stehouwer CD, Serné EH, Poel DM, Groot L, Kager C et al (2009) Microvascular function has no menstrual-cycle-dependent variation in healthy ovulatory women. Microcirculation 16:714–724
Kim ESH, Menon V (2009) Status of women in cardiovascular clinical trials. Arterioscler Thromb Vasc Biol 29:279–283. https://doi.org/10.1161/ATVBAHA.108.179796
King TJ, Pyke KE (2019) Evidence of a limb- and shear stress stimulus profile-dependent impact of high-intensity cycling training on flow-mediated dilation. Appl Physiol Nutr Metab 45:135–145. https://doi.org/10.1139/apnm-2019-0151
King TJ, Schmitter SM, Pyke KE (2017) Assessment of flow-mediated dilatation in the superficial femoral artery using a sustained shear stress stimulus via calf plantar-flexion exercise. Exp Physiol 102:725–737. https://doi.org/10.1113/ep085980
Lind L, Berglund L, Larsson A, Sundström J (2011) Endothelial function in resistance and conduit arteries and 5-year risk of cardiovascular disease. Circulation 123:1545–1551. https://doi.org/10.1161/CIRCULATIONAHA.110.984047
Liu KR, Lew LA, McGarity-Shipley EC, Byrne AC, Islam H, Fenuta AM et al (2021) Individual variation of follicular phase changes in endothelial function across two menstrual cycles. Exp Physiol. https://doi.org/10.1113/EP089482
Mullen MJ, Kharbanda RK, Cross J, Donald AE, Taylor M, Vallance P et al (2001) Heterogenous nature of flow-mediated dilatation in human conduit arteries in vivo. Circ Res 88:145–151. https://doi.org/10.1161/01.RES.88.2.145
Naylor LH, Carter H, FitzSimons MG, Cable NT, Thijssen DHJ, Green DJ (2011) Repeated increases in blood flow, independent of exercise, enhance conduit artery vasodilator function in humans. Am J Physiol Heart Circ Physiol 300:H664–H669. https://doi.org/10.1152/ajpheart.00985.2010
Newcomer SC, Leuenberger UA, Hogeman CS, Handly BD, Proctor DN (2004) Different vasodilator responses of human arms and legs. J Physiol 556:1001–1011. https://doi.org/10.1113/jphysiol.2003.059717
O’Driscoll G, Green D, Rankin J, Stanton K, Taylor R (1997a) Improvement in endothelial function by angiotensin converting enzyme inhibition in insulin-dependent diabetes mellitus. J Clin Invest 100:678–684. https://doi.org/10.1172/JCI119580
O’Driscoll G, Green D, Taylor RR (1997b) Simvastatin, an HMG coenzyme a reductase inhibitor, improves endothelial function within 1 month. Circulation 95:1126–1131. https://doi.org/10.1161/01.CIR.95.5.1126
Padilla J, Newcomer SC, Simmons GH, Kreutzer KV, Laughlin MH (2010) Long-term exercise training does not alter brachial and femoral artery vasomotor function and endothelial phenotype in healthy pigs. Am J Physiol Heart Circ Physiol 299:H379-385. https://doi.org/10.1152/ajpheart.00294.2010
Pierce GL, Eskurza I, Walker AE, Fay TN, Seals DR (2011) Sex-specific effects of habitual aerobic exercise on brachial artery flow-mediated dilation in middle-aged and older adults. Clin Sci (lond) 120:13–23. https://doi.org/10.1042/cs20100174
Pyke KE, Tschakovsky ME (2007) Peak vs. Total reactive hyperemia: which determines the magnitude of flow-mediated dilation? J Appl Physiol 102:1510–1519. https://doi.org/10.1152/japplphysiol.01024.2006
Pyke KE, Poitras V, Tschakovsky ME (2008a) 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. https://doi.org/10.1152/ajpheart.01372.2007
Pyke KE, Hartnett JA, Tschakovsky ME (2008b) Are the dynamic response characteristics of brachial artery flow-mediated dilation sensitive to the magnitude of increase in shear stimulus? J Appl Physiol 105:282–292. https://doi.org/10.1152/japplphysiol.01190.2007
Radak Z, Chung HY, Koltai E, Taylor AW, Goto S (2008) Exercise, oxidative stress and hormesis. Ageing Res Rev 7:34–42. https://doi.org/10.1016/j.arr.2007.04.004
Rakobowchuk M, Tanguay S, Burgomaster KA, Howarth KR, Gibala MJ, MacDonald MJ (2008) Sprint interval and traditional endurance training induce similar improvements in peripheral arterial stiffness and flow-mediated dilation in healthy humans. Am J Physiol Regul Integr Comp Physiol 295:R236–R242. https://doi.org/10.1152/ajpregu.00069.2008
Romero SA, Gagnon D, Adams AN, Cramer MN, Kouda K, Crandall CG (2017) Acute limb heating improves macro-and microvascular dilator function in the leg of aged humans. Am J Physiol Heart Circ Physiol 312:H89–H97. https://doi.org/10.1152/ajpheart.00519.2016
Schaumberg MA, Jenkins DG, Janse de Jonge XAK, Emmerton LM, Skinner TL (2017) Three-step method for menstrual and oral contraceptive cycle verification. J Sci Med Sport 20:965–969. https://doi.org/10.1016/j.jsams.2016.08.013
Scholten RR, Thijssen DJH, Lotgering FK, Hopman MTE, Spaanderman MEA (2014) Cardiovascular effects of aerobic exercise training in formerly preeclamptic women and healthy parous control subjects. Am J Obstet Gynecol 211:516.e511-516.e511. https://doi.org/10.1016/j.ajog.2014.04.025
Sheel AW (2016) Sex differences in the physiology of exercise: an integrative perspective. Exp Physiol 101:211–212. https://doi.org/10.1113/EP085371
Shenouda N, Priest SE, Rizzuto VI, MacDonald MJ (2018) Brachial artery endothelial function is stable across a menstrual and oral contraceptive pill cycle but lower in premenopausal women than in age-matched men. Am J Physiol Heart Circ Physiol 315:H366–H374. https://doi.org/10.1152/ajpheart.00102.2018
Shu J, Santulli G (2018) Update on peripheral artery disease: Epidemiology and evidence-based facts. Atherosclerosis 275:379–381. https://doi.org/10.1016/j.atherosclerosis.2018.05.033
Slattery DJ, Stuckless TJR, King TJ, Pyke KE (2016) Impaired handgrip exercise-induced brachial artery flow-mediated dilation in young obese males. Appl Physiol Nutr Metab 41:528–537. https://doi.org/10.1139/apnm-2015-0459
Spence AL, Carter HH, Naylor LH, Green DJ (2013) A prospective randomized longitudinal study involving 6 months of endurance or resistance exercise. Conduit artery adaptation in humans. J Physiol 591:1265–1275. https://doi.org/10.1113/jphysiol.2012.247387
Sun D, Huang A, Koller A, Kaley G (1998) Adaptation of flow-induced dilation of arterioles to daily exercise. Microvasc Res 56:54–61. https://doi.org/10.1006/mvre.1998.2083
Thijssen DHJ, De Groot PCE, Smits P, Hopman MTE (2007) Vascular adaptations to 8-week cycling training in older men. Acta Physiol 190:221–228. https://doi.org/10.1111/j.1748-1716.2007.01685.x
Thijssen DHJ, Black MA, Pyke KE, Padilla J, Atkinson G, Harris RA et al (2011) Assessment of flow-mediated dilation in humans: a methodological and physiological guideline. Am J Physiol Heart Circ Physiol 300:H2–H12. https://doi.org/10.1152/ajpheart.00471.2010
Thomas KN, van Rij AM, Lucas SJE, Gray AR, Cotter JD (2016) Substantive hemodynamic and thermal strain upon completing lower-limb hot-water immersion; comparisons with treadmill running. Temperature 3:286–297. https://doi.org/10.1080/23328940.2016.1156215
Tinken TM, Thijssen DHJ, 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. https://doi.org/10.1113/jphysiol.2008.158014
Tinken TM, Thijssen DHJ, Hopkins N, Black MA, Dawson EA, Minson CT et al (2009) Impact of shear rate modulation on vascular function in humans. Hypertension 54:278–285. https://doi.org/10.1161/HYPERTENSIONAHA.109.134361
Tinken TM, Thijssen DH, Hopkins N, Dawson EA, Cable NT, Green DJ (2010) Shear stress mediates endothelial adaptations to exercise training in humans. Hypertension 55:312–318. https://doi.org/10.1161/HYPERTENSIONAHA.109.146282
Totosy de Zepetnek JO, Jermey TL, MacDonald MJ (2014) Superficial femoral artery endothelial responses to a short-term altered shear rate intervention in healthy men. PLoS ONE 9:e113407. https://doi.org/10.1371/journal.pone.0113407
Tremblay JC, Pyke KE (2018) Flow-mediated dilation stimulated by sustained increases in shear stress: a useful tool for assessing endothelial function in humans? Am J Physiol Heart Circ Physiol 314:H508–H520. https://doi.org/10.1152/ajpheart.00534.2017
Tremblay MS, Warburton DER, Janssen I, Paterson DH, Latimer AE, Rhodes RE et al (2011) New canadian physical activity guidelines. Appl Physiol Nutr Metab 36:36–46. https://doi.org/10.1139/h11-009
Tremblay JC, Stimpson TV, Pyke KE (2019a) Evidence of sex differences in the acute impact of oscillatory shear stress on endothelial function. J Appl Physiol 126:314–321. https://doi.org/10.1152/japplphysiol.00729.2018
Tremblay JC, Williams JS, Pyke KE (2019b) Ramp and step increases in shear stress result in a similar magnitude of brachial artery flow-mediated dilation. Eur J Appl Physiol 119:611–619. https://doi.org/10.1007/s00421-018-4049-y
Vranish JR, Young BE, Kaur J, Patik JC, Padilla J, Fadel PJ (2017a) Influence of sex on microvascular and macrovascular responses to prolonged sitting. Am J Physiol Heart Circ Physiol 312:H800-h805. https://doi.org/10.1152/ajpheart.00823.2016
Williams JS, Stimpson TV, Tremblay JC, Fenuta AM, Pyke KE (2019) The influence of acute hyperglycaemia on brachial artery flow-mediated dilatation in the early and late follicular phases of the menstrual cycle. Exp Physiol 104:957–966. https://doi.org/10.1113/EP087536
Wilson R, Adams ML, Pyke KE (2020) Inclusion of female participants in cardiovascular research: a case study of Ontario NSERC-funded programs. Appl Physiol Nutr Metab 45:911–914. https://doi.org/10.1139/apnm-2019-0693
Wray DW, Uberoi A, Lawrenson L, Richardson RS (2005) Heterogeneous limb vascular responsiveness to shear stimuli during dynamic exercise in humans. J Appl Physiol 99:81–86. https://doi.org/10.1152/japplphysiol.01285.2004
Wray DW, Witman MAH, Ives SJ, McDaniel J, Fjeldstad AS, Trinity JD et al (2011) Progressive handgrip exercise: Evidence of nitric oxide-dependent vasodilation and blood flow regulation in humans. Am J Physiol Heart Circ Physiol 300:H1101–H1107. https://doi.org/10.1152/ajpheart.01115.2010
Wu SP, Ringgaard S, Oyre S, Hansen MS, Rasmus S, Pedersen EM (2004) Wall shear rates differ between the normal carotid, femoral, and brachial arteries: an in vivo MRI study. J Magn Reson Imaging 19:188–193. https://doi.org/10.1002/jmri.10441
Yanovich R, Ketko I, Charkoudian N (2020) Sex differences in human thermoregulation: relevance for 2020 and beyond. Physiology 35:177–184. https://doi.org/10.1152/physiol.00035.2019
Acknowledgements
The authors would like to acknowledge Dr. Robert Ross and his research team for providing the accelerometers and assisting with data analysis.
Funding
This study was funded by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant, and by Canada Foundation for Innovation and Ontario Ministry of Research and Innovation Leaders Opportunity Funding to KE Pyke. EC McGarity-Shipley was supported by an RS McLaughlin Fellowship. S Schmitter and I McPhee were supported by a Ministry of Research Innovation Early Researcher Award to KE Pyke. TJ King was supported by an NSERC PGS D fellowship.
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SMS and KEP conceived and designed the research. ECM and SMS lead data collection, analyzed the data and drafted the manuscript with editing by KEP. JSW, TJK and IACM. JSW, TJK, and IACM participated in data collection and analysis. All authors read and approved the final manuscript.
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McGarity-Shipley, E.C., Schmitter, S.M., Williams, J.S. et al. The impact of repeated, local heating-induced increases in blood flow on lower limb endothelial function in young, healthy females. Eur J Appl Physiol 121, 3017–3030 (2021). https://doi.org/10.1007/s00421-021-04749-7
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DOI: https://doi.org/10.1007/s00421-021-04749-7