Advertisement

Effect of external compression on femoral retrograde shear and microvascular oxygenation in exercise trained and recreationally active young men

  • Patricia Pagan Lassalle
  • Adam J. Palamar
  • Jacob P. DeBlois
  • Wesley K. Lefferts
  • Kevin S. HeffernanEmail author
Original Article

Abstract

Introduction

Retrograde shear causes endothelial damage and is pro-atherogenic. The purpose of our study was to examine the impact of vascular remodeling from habitual exercise training on acute changes in retrograde shear and microvascular oxygenation (SMO2) induced via 30 min of external compression.

Methods

Participants included 11 exercise trained (ET) men (Division I track athletes; age 20 ± 3 years) and 18 recreationally active (RA) men (age 23 ± 5 years). Near-infrared spectroscopy (NIRS) was used to measure vastus medialis SMO2. Doppler-ultrasound was used to assess SFA intima-media thickness, diameter and flow velocity to derive retrograde shear. Vascular measures were made at baseline (BASELINE), during a sham condition (calf compression to 5 mmHg, SHAM) and during the experimental condition (calf compression to 60 mmHg, EXP).

Results

Compared to RA, ET had larger SFA diameters (0.66 ± 0.06 vs 0.58 ± 0.06 cm, p < 0.05) and lower SFA IMT (0.33 ± 0.03 vs 0.36 ± 0.07 mm, p < 0.05). Retrograde shear increased similarly in both groups during EXP (p < 0.05) but ET men had lower overall retrograde shear during the conditions (BASELINE 75.8 ± 26.8 vs EXP 88.2 ± 16.9 s−1) compared to RA men (BASELINE 84.4 ± 23.3 vs EXP 106.4 ± 19.6 s−1p < 0.05). There was a similar increase in SMO2 from BASELINE to SHAM (ET + 8.1 ± 4.8 vs RA + 6.4 ± 9.7%) and BASELINE to EXP (ET + 8.7 ± 6.4 vs RA + 7.1 ± 9.0%) in both groups.

Conclusion

Beneficial vascular remodeling in ET men is associated with lower retrograde shear during external compression. Acute increases in retrograde shear with external compression do not detrimentally impact microvascular oxygenation.

Keywords

Retrograde shear Vascular Arterial stiffness Exercise training 

Abbreviations

BMI

Body mass index

DBP

Diastolic blood pressure

ET

Exercise-trained

HR

Heart rate

IPAQ

International Physical Activity Questionnaire

IMT

Intima-media thickness

SMO2

Muscle oxygen saturation

NIRS

Near-infrared spectroscopy

PWV

Pulse wave velocity

RA

Recreationally active

SV

Stroke volume

SFA

Superficial femoral artery

SBP

Systolic blood pressure

Notes

Author contributions

All authors conceptualized the study and assisted with study design. All authors piloted data collection. All authors prepared documents for ethics review (university IRB). PPL and AJP recruited all participants and collected all data. JPD and WKL oversaw all data collection to ensure high-quality data acquisition. PPL and AJP reduced all data and entered data into spreadsheets. JPD, WKL, and KSH conducted statistical analyses and interpreted results. PPL prepared data tables. All authors assisted with the preparation of the final manuscript. JPD and WKL edited all versions for scientific accuracy and overall presentation.

References

  1. Augustine JA, Lefferts WK, Dowthwaite JN, Brann LS, Brutsaert TD, Heffernan KS (2016) Subclinical atherosclerotic risk in endurance-trained premenopausal amenorrheic women. Atherosclerosis 244:157–164CrossRefGoogle Scholar
  2. Bell PL, Kelley ET, McCoy SM, Credeur DP (2017) Influence of aerobic fitness on vasoreactivity in young men. Eur J Appl Physiol 117:2075–2083CrossRefGoogle Scholar
  3. Breton-Romero R, Wang N, Palmisano J, Larson MG, Vasan RS, Mitchell GF, Benjamin EJ, Vita JA, Hamburg NM (2016) Cross-sectional associations of flow reversal, vascular function, and arterial stiffness in the framingham heart study. Arterioscler Thromb Vasc Biol 36:2452–2459CrossRefGoogle Scholar
  4. Casey DP, Padilla J, Joyner MJ (2012) Alpha-adrenergic vasoconstriction contributes to the age-related increase in conduit artery retrograde and oscillatory shear. Hypertension (Dallas, Tex: 1979) 60:1016–1022CrossRefGoogle Scholar
  5. Casey DP, Schneider AC, Ueda K (2016) Influence of chronic endurance exercise training on conduit artery retrograde and oscillatory shear in older adults. Eur J Appl Physiol 116:1931–1940CrossRefGoogle Scholar
  6. Crum EM, O'Connor WJ, Van Loo L, Valckx M, Stannard SR (2017) Validity and reliability of the Moxy oxygen monitor during incremental cycling exercise. Eur J Sport Sci 17:1037–1043CrossRefGoogle Scholar
  7. 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:e113407CrossRefGoogle Scholar
  8. de Zepetnek JO, Ditor DS, Au JS, MacDonald MJ (2015) Impact of shear rate pattern on upper and lower limb conduit artery endothelial function in both spinal cord-injured and able-bodied men. Exp Physiol 100:1107–1117CrossRefGoogle Scholar
  9. Dinenno FA, Jones PP, Seals DR, Tanaka H (2000) Age-associated arterial wall thickening is related to elevations in sympathetic activity in healthy humans. Am J Physiol Heart Circ Physiol 278:H1205–1210CrossRefGoogle Scholar
  10. Dinenno FA, Tanaka H, Monahan KD, Clevenger CM, Eskurza I, DeSouza CA, Seals DR (2001) Regular endurance exercise induces expansive arterial remodelling in the trained limbs of healthy men. J Physiol 534:287–295CrossRefGoogle Scholar
  11. Feistritzer HJ, Reinstadler SJ, Klug G, Kremser C, Seidner B, Esterhammer R, Schocke MF, Franz WM, Metzler B (2015) Comparison of an oscillometric method with cardiac magnetic resonance for the analysis of aortic pulse wave velocity. PLoS ONE 10:e0116862CrossRefGoogle Scholar
  12. Freire CM, Ribeiro AL, Barbosa FB, Nogueira AL, Almeida MC, de Barbosa MM, Lana AM, de Silva AC, Ribeiro-Oliveira A (2009) Comparison between automated and manual measurements of carotid intima-media thickness in clinical practice. Vasc Health Risk Manag 5:811–817Google Scholar
  13. Green DJ, Spence A, Rowley N, Thijssen DH, Naylor LH (2012) Vascular adaptation in athletes: is there an 'athlete's artery'? Exp Physiol 97:295–304CrossRefGoogle Scholar
  14. Halliwill JR, Minson CT (2010) Retrograde shear: backwards into the future? Am J Physiol Heart Circ Physiol 298:H1126–1127CrossRefGoogle Scholar
  15. Hashimoto J, Ito S (2010) Pulse pressure amplification, arterial stiffness, and peripheral wave reflection determine pulsatile flow waveform of the femoral artery. Hypertension (Dallas, Tex: 1979) 56:926–933CrossRefGoogle Scholar
  16. Heffernan KS, Lefferts WK, Kasprowicz AG, Tarzia BJ, Thijssen DH, Brutsaert TD (2013) Manipulation of arterial stiffness, wave reflections, and retrograde shear rate in the femoral artery using lower limb external compression. Physiol Rep 1:e00022CrossRefGoogle Scholar
  17. Helmerhorst HJ, Brage S, Warren J, Besson H, Ekelund U (2012) A systematic review of reliability and objective criterion-related validity of physical activity questionnaires. Int J Behav Nutr Phys Activity 9:103CrossRefGoogle Scholar
  18. Hughes WE, Ueda K, Casey DP (2016) Chronic endurance exercise training offsets the age-related attenuation in contraction-induced rapid vasodilation. J Appl Physiol (Bethesda, Md: 1985) 120:1335–1342CrossRefGoogle Scholar
  19. Ives SJ, Fadel PJ, Brothers RM, Sander M, Wray DW (2014) Exploring the vascular smooth muscle receptor landscape in vivo: ultrasound Doppler versus near-infrared spectroscopy assessments. Am J Physiol Heart Circ Physiol 306:H771–776CrossRefGoogle Scholar
  20. Johnson BD, Mather KJ, Newcomer SC, Mickleborough TD, Wallace JP (2012) Brachial artery flow-mediated dilation following exercise with augmented oscillatory and retrograde shear rate. Cardiovasc Ultras 10:34CrossRefGoogle Scholar
  21. Jones CR, Taylor K, Chowienczyk P, Poston L, Shennan AH (2000) A validation of the Mobil O Graph (version 12) ambulatory blood pressure monitor. Blood Pressure Monit 5:233–238CrossRefGoogle Scholar
  22. Jones S, Chiesa ST, Chaturvedi N, Hughes AD (2016) Recent developments in near-infrared spectroscopy (NIRS) for the assessment of local skeletal muscle microvascular function and capacity to utilise oxygen. Artery research 16:25–33CrossRefGoogle Scholar
  23. McManus CJ, Collison J, Cooper CE (2018) Performance comparison of the MOXY and PortaMon near-infrared spectroscopy muscle oximeters at rest and during exercise. J Biomed Opt 23:1–14CrossRefGoogle Scholar
  24. Moreau KL, Silver AE, Dinenno FA, Seals DR (2006) Habitual aerobic exercise is associated with smaller femoral artery intima-media thickness with age in healthy men and women. Eur J Cardiovasc Prevent Rehabilit 13:805–811CrossRefGoogle Scholar
  25. Nichols S, Milner M, Meijer R, Carroll S, Ingle L (2016) Variability of automated carotid intima-media thickness measurements by novice operators. Clin Physiol Funct Imaging 36:25–32CrossRefGoogle Scholar
  26. Padilla J, Sheldon RD, Sitar DM, Newcomer SC (2009) Impact of acute exposure to increased hydrostatic pressure and reduced shear rate on conduit artery endothelial function: a limb-specific response. Am J Physiol Heart Circ Physiol 297:H1103–1108CrossRefGoogle Scholar
  27. Ramos Gonzalez M, Caldwell JT, Branch PA, Wardlow GC, Black CD, Campbell J, Larson RD, Ade CJ (2018) Impact of shear rate pattern on post-occlusive near-infrared spectroscopy microvascular reactivity. Microvasc Res 116:50–56CrossRefGoogle Scholar
  28. Restaino RM, Walsh LK, Morishima T, Vranish JR, Martinez-Lemus LA, Fadel PJ, Padilla J (2016) Endothelial dysfunction following prolonged sitting is mediated by a reduction in shear stress. Am J Physiol Heart Circ Physiol 310:H648–653CrossRefGoogle Scholar
  29. Schreuder TH, Green DJ, Hopman MT, Thijssen DH (2014) Acute impact of retrograde shear rate on brachial and superficial femoral artery flow-mediated dilation in humans. Physiol Rep 2:e00193CrossRefGoogle Scholar
  30. Schreuder TH, Green DJ, Hopman MT, Thijssen DH (2015) Impact of retrograde shear rate on brachial and superficial femoral artery flow-mediated dilation in older subjects. Atherosclerosis 241:199–204CrossRefGoogle Scholar
  31. Tanahashi K, Kosaki K, Sawano Y, Yoshikawa T, Tagawa K, Kumagai H, Akazawa N, Maeda S (2017) Impact of age and aerobic exercise training on conduit artery wall thickness: role of the shear pattern. J Vasc Res 54:272–279CrossRefGoogle Scholar
  32. Thijssen DH, Dawson EA, Tinken TM, Cable NT, Green DJ (2009) Retrograde flow and shear rate acutely impair endothelial function in humans. Hypertension (Dallas, Tex: 1979) 53:986–992CrossRefGoogle Scholar
  33. Thijssen DH, Scholten RR, van den Munckhof IC, Benda N, Green DJ, Hopman MT (2011) Acute change in vascular tone alters intima-media thickness. Hypertension (Dallas, Tex: 1979) 58:240–246CrossRefGoogle Scholar
  34. Thijssen DH, Atkinson CL, Ono K, Sprung VS, Spence AL, Pugh CJ, Green DJ (2014) Sympathetic nervous system activation, arterial shear rate, and flow-mediated dilation. J Appl Physiol (Bethesda, Md: 1985) 116:1300–1307CrossRefGoogle Scholar
  35. Thijssen DH, Schreuder TH, Newcomer SW, Laughlin MH, Hopman MT, Green DJ (2015) Impact of 2-weeks continuous increase in retrograde shear stress on brachial artery vasomotor function in young and older men. J Am Heart Assoc 4:e001968CrossRefGoogle Scholar
  36. 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 (Dallas, Tex: 1979) 54:278–285CrossRefGoogle Scholar
  37. Tremblay JC, Stimpson TV, Pyke KE (2018) Evidence of sex differences in the acute impact of oscillatory shear stress on endothelial function. J Appl Physiol (Bethesda, Md: 1985) 126(2):314–321CrossRefGoogle Scholar
  38. Tucker WJ, Rosenberry R, Trojacek D, Chamseddine HH, Arena-Marshall CA, Zhu Y, Wang J, Kellawan JM, Haykowsky MJ, Tian F, Nelson MD (2019) Studies into the determinants of skeletal muscle oxygen consumption: novel insight from near-infrared diffuse correlation spectroscopy. J Physiol 597(11):2887–2901CrossRefGoogle Scholar
  39. Weber T, Wassertheurer S, Rammer M, Maurer E, Hametner B, Mayer CC, Kropf J, Eber B (2011) Validation of a brachial cuff-based method for estimating central systolic blood pressure. Hypertension (Dallas, Tex: 1979) 58:825–832CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Patricia Pagan Lassalle
    • 1
  • Adam J. Palamar
    • 1
  • Jacob P. DeBlois
    • 1
  • Wesley K. Lefferts
    • 1
  • Kevin S. Heffernan
    • 1
    Email author
  1. 1.Department of Exercise ScienceThe Human Performance Laboratory, Syracuse UniversitySyracuseUSA

Personalised recommendations