Advertisement

European Journal of Applied Physiology

, Volume 118, Issue 6, pp 1209–1219 | Cite as

Perfusion dynamics assessment with Power Doppler ultrasound in skeletal muscle during maximal and submaximal cycling exercise

  • H. M. Heres
  • T. Schoots
  • B. C. Y. Tchang
  • M. C. M. Rutten
  • H. M. C. Kemps
  • F. N. van de Vosse
  • R. G. P. Lopata
Original Article

Abstract

Purpose

Assessment of limitations in the perfusion dynamics of skeletal muscle may provide insight in the pathophysiology of exercise intolerance in, e.g., heart failure patients. Power doppler ultrasound (PDUS) has been recognized as a sensitive tool for the detection of muscle blood flow. In this volunteer study (N = 30), a method is demonstrated for perfusion measurements in the vastus lateralis muscle, with PDUS, during standardized cycling exercise protocols, and the test–retest reliability has been investigated.

Methods

Fixation of the ultrasound probe on the upper leg allowed for continuous PDUS measurements. Cycling exercise protocols included a submaximal and an incremental exercise to maximal power. The relative perfused area (RPA) was determined as a measure of perfusion. Absolute and relative reliability of RPA amplitude and kinetic parameters during exercise (onset, slope, maximum value) and recovery (overshoot, decay time constants) were investigated.

Results

A RPA increase during exercise followed by a signal recovery was measured in all volunteers. Amplitudes and kinetic parameters during exercise and recovery showed poor to good relative reliability (ICC ranging from 0.2–0.8), and poor to moderate absolute reliability (coefficient of variation (CV) range 18–60%).

Conclusions

A method has been demonstrated which allows for continuous (Power Doppler) ultrasonography and assessment of perfusion dynamics in skeletal muscle during exercise. The reliability of the RPA amplitudes and kinetics ranges from poor to good, while the reliability of the RPA increase in submaximal cycling (ICC = 0.8, CV = 18%) is promising for non-invasive clinical assessment of the muscle perfusion response to daily exercise.

Keywords

Power Doppler ultrasound Perfusion Exercise Skeletal muscle Test–retest reliability Probe fixation 

Abbreviations

AT

Anaerobic threshold

CEUS

Contrast-enhanced ultrasound

CPET

Cardiopulmonary exercise test

CV

Coefficient of variation

ECG

Electrocardiogram

ICC

Intraclass coefficient

MRT

Mean response time

PDUS

Power Doppler ultrasound

PRF

Pulse repetition frequency

ROI

Region of interest

RPA

Relative perfused area

Notes

Acknowledgements

This study was funded by the European Community’s Seventh Framework Programme (FP7/2007–2013) under Grant Agreement No. 318067.

Author contribution statement

MH, TS, HK, and RL conceived and designed the research. MH and TS conducted experiments and analyzed data. BT contributed to analytical and experimental tools. RL, FV and MR helped supervise the project. MH wrote the manuscript. All authors read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

No conflicts of interest, financial or otherwise, are declared by the authors.

References

  1. Alcázar JL (2008) Three-dimensional power Doppler derived vascular indices: What are we measuring and how are we doing it? Ultrasound Obstet Gynecol 32:485–487.  https://doi.org/10.1002/uog.6144 CrossRefPubMedGoogle Scholar
  2. Atkinson G, Nevill A (1998) Statistical methods for assssing measurement error (reliability) in variables relevant to sports medicine. Sport Med 26:217–238.  https://doi.org/10.2165/00007256-199826040-00002 CrossRefGoogle Scholar
  3. Calbet J, Lundby L C (2012) Skeletal muscle vasodilatation during maximal exercise in health and disease. J Physiol 590:6285–6296.  https://doi.org/10.1113/jphysiol.2012.241190 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Calbet JAL, Gonzalez-Alonso J, Helge JW et al (2007) Cardiac output and leg and arm blood flow during incremental exercise to exhaustion on the cycle ergometer. J Appl Physiol 103:969–978.  https://doi.org/10.1152/japplphysiol.01281.2006 CrossRefPubMedGoogle Scholar
  5. Cosgrove D, Lassau N (2010) Imaging of perfusion using ultrasound. Eur J Nucl Med Mol Imaging 37:65–85.  https://doi.org/10.1007/s00259-010-1537-7 CrossRefGoogle Scholar
  6. Dori A, Abbasi H, Zaidman CM (2016) Intramuscular blood flow quantification with power Doppler ultrasonography. Muscle Nerve 54:872–878.  https://doi.org/10.1002/mus.25108 CrossRefPubMedGoogle Scholar
  7. Dubiel M, Kozber H, Debniak B et al (1999) Fetal and placental power Doppler imaging in normal and high-risk pregnancy. Eur J Ultrasound 9:223–230.  https://doi.org/10.1016/S0929-8266(99)00027-0 CrossRefPubMedGoogle Scholar
  8. Esposito F, Mathieu-Costello O, Shabetai R et al (2010) Limited maximal exercise capacity in patients with chronic heart failure. J Am Coll Cardiol 55:1945–1954.  https://doi.org/10.1016/j.jacc.2009.11.086 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Green S, Thorp R, Reeder EJ et al (2011) Venous occlusion plethysmography versus Doppler ultrasound in the assessment of leg blood flow during calf exercise. Eur J Appl Physiol 111:1889–1900.  https://doi.org/10.1007/s00421-010-1819-6 CrossRefPubMedGoogle Scholar
  10. Harold Laughlin M, Davis MJ, Secher NH et al (2012) Peripheral circulation. Compr Physiol 2:321–447.  https://doi.org/10.1002/cphy.c100048 CrossRefPubMedGoogle Scholar
  11. Heinonen I, Koga S, Kalliokoski KK et al (2015) Heterogeneity of muscle blood flow and metabolism. Exerc Sport Sci Rev.  https://doi.org/10.1249/JES.0000000000000044 PubMedPubMedCentralCrossRefGoogle Scholar
  12. Hernandez-Andrade E, Jansson T, Ley D et al (2004) Validation of fractional moving blood volume measurement with power Doppler ultrasound in an experimental sheep model. Ultrasound Obstet Gynecol 23:363–368.  https://doi.org/10.1002/uog.1002 CrossRefPubMedGoogle Scholar
  13. Joshua F, Edmonds J, Lassere M (2006) Power doppler ultrasound in musculoskeletal disease: a systematic review. Semin Arthritis Rheum 36:99–108.  https://doi.org/10.1016/j.semarthrit.2006.04.009 CrossRefPubMedGoogle Scholar
  14. Kemps HMC, Prompers JJ, Wessels B et al (2009) Skeletal muscle metabolic recovery following submaximal exercise in chronic heart failure is limited more by O2 delivery than O2 utilization. Clin Sci 118:203–210.  https://doi.org/10.1042/CS20090220 CrossRefPubMedGoogle Scholar
  15. Kerschan-Schindl K, Grampp S, Henk C et al (2001) Whole-body vibration exercise leads to alterations in muscle blood volume. Clin Physiol 21:377–382.  https://doi.org/10.1046/j.1365-2281.2001.00335.x CrossRefPubMedGoogle Scholar
  16. Krix M, Weber M-A, Krakowski-Roosen H et al (2005) Assessment of skeletal muscle perfusion using contrast-enhanced ultrasonography. J Ultrasound Med 24:431–441CrossRefPubMedGoogle Scholar
  17. Krix M, Krakowski-Roosen H, Kauczor HU et al (2009) Real-time contrast-enhanced ultrasound for the assessment of perfusion dynamics in skeletal muscle. Ultrasound Med Biol 35:1587–1595.  https://doi.org/10.1016/j.ultrasmedbio.2009.05.006 CrossRefPubMedGoogle Scholar
  18. Krix M, Krakowski-Roosen H, Armarteifio E et al (2011) Comparison of transient arterial occlusion and muscle exercise provocation for assessment of perfusion reserve in skeletal muscle with real-time contrast-enhanced ultrasound. Eur J Radiol 78:419–424.  https://doi.org/10.1016/j.ejrad.2009.11.014 CrossRefPubMedGoogle Scholar
  19. Murias JM, Spencer MD, Keir DA, Paterson DH (2013) Systemic and vastus lateralis muscle blood flow and O2 extraction during ramp incremental cycle exercise. AJP Regul Integr Comp Physiol 304:R720–R725.  https://doi.org/10.1152/ajpregu.00016.2013 CrossRefGoogle Scholar
  20. Newman JS, Adler R, Rubin JM (1997) Power Doppler sonography: use in measuring alterations in muscle blood volume after exercise. J Diagnostic Med Sonogr 13:266–266.  https://doi.org/10.1177/875647939701300527 CrossRefGoogle Scholar
  21. Poole DC, Jones AM (2012) Oxygen uptake kinetics. Compr Physiol 2:933–996.  https://doi.org/10.1002/cphy.c100072 PubMedCrossRefGoogle Scholar
  22. Poole DC, Hirai DM, Copp SW, Musch TI (2012) Muscle oxygen transport and utilization in heart failure: implications for exercise (in)tolerance. Am J Physiol Circ Physiol 302:H1050–H1063.  https://doi.org/10.1152/ajpheart.00943.2011 CrossRefGoogle Scholar
  23. Raine-Fenning NJ, Nordin NM, Ramnarine KV et al (2008) Determining the relationship between three-dimensional power Doppler data and true blood flow characteristics: an in-vitro flow phantom experiment. Ultrasound Obstet Gynecol 32:540–550.  https://doi.org/10.1002/uog.6110 CrossRefPubMedGoogle Scholar
  24. Rubin JM, Bude RO, Carson PL et al (1994) Power Doppler US: a potentially useful alternative to mean frequency-based color Doppler US. Radiology 190:853–856.  https://doi.org/10.1148/radiology.190.3.8115639 CrossRefPubMedGoogle Scholar
  25. Santamaría G, Velasco M, Farré X et al (2005) Power doppler sonography of invasive breast carcinoma: does tumor vascularization contribute to prediction of axillary status? Radiology 234:374–380.  https://doi.org/10.1148/radiol.2342031252 CrossRefPubMedGoogle Scholar
  26. Schep G, Bender MHM, Van de Tempel G et al (2002) Detection and treatment of claudication due to functional iliac obstruction in top endurance athletes: a prospective study. Lancet 359:466–473.  https://doi.org/10.1016/S0140-6736(02)07675-4 CrossRefPubMedGoogle Scholar
  27. Spee RF, Niemeijer VM, Wessels B et al (2015) Characterization of exercise limitations by evaluating individual cardiac output patterns: a prospective cohort study in patients with chronic heart failure. BMC Cardiovasc Disord 15:57.  https://doi.org/10.1186/s12872-015-0057-6 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Sullivan MJ, Hawthorne MH (1995) Exercise intolerance in patients with chronic heart failure. Prog Cardiovasc Dis 38:1–22.  https://doi.org/10.1016/S0033-0620(05)80011-8 CrossRefPubMedGoogle Scholar
  29. Thomas KN, Cotter JD, Lucas SJE et al (2015) Reliability of contrast-enhanced ultrasound for the assessment of muscle perfusion in health and peripheral arterial disease. Ultrasound Med Biol 41:26–34.  https://doi.org/10.1016/j.ultrasmedbio.2014.06.012 CrossRefPubMedGoogle Scholar
  30. Thompson RB, Pagano JJ, Mathewson KW et al (2016) Differential responses of post-exercise recovery of leg blood flow and oxygen uptake kinetics in HFpEF versus HFrEF. PLoS One 11:1–14.  https://doi.org/10.1371/journal.pone.0163513 CrossRefGoogle Scholar
  31. Welsh A (2004) Quantification of power Doppler and the index “fractional moving blood volume” (FMBV). Ultrasound Obstet Gynecol 23:323–326.  https://doi.org/10.1002/uog.1037 CrossRefPubMedGoogle Scholar
  32. Wortsman X (2012) Common applications of dermatologic sonography. J Ultrasound Med 31:97–111.  https://doi.org/10.7863/jum.2012.31.1.97 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Cardiovascular Biomechanics Group, Department of Biomedical EngineeringEindhoven University of TechnologyEindhovenThe Netherlands
  2. 2.Department of CardiologyMáxima Medical CentreVeldhovenThe Netherlands

Personalised recommendations