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.
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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
References
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
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
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
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
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
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
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
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
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
Harold Laughlin M, Davis MJ, Secher NH et al (2012) Peripheral circulation. Compr Physiol 2:321–447. https://doi.org/10.1002/cphy.c100048
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
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
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
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
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
Krix M, Weber M-A, Krakowski-Roosen H et al (2005) Assessment of skeletal muscle perfusion using contrast-enhanced ultrasonography. J Ultrasound Med 24:431–441
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
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
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
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
Poole DC, Jones AM (2012) Oxygen uptake kinetics. Compr Physiol 2:933–996. https://doi.org/10.1002/cphy.c100072
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
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
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
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
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
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
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
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
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
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
Wortsman X (2012) Common applications of dermatologic sonography. J Ultrasound Med 31:97–111. https://doi.org/10.7863/jum.2012.31.1.97
Acknowledgements
This study was funded by the European Community’s Seventh Framework Programme (FP7/2007–2013) under Grant Agreement No. 318067.
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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.
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Communicated by I. Mark Olfert.
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Heres, H.M., Schoots, T., Tchang, B.C.Y. et al. Perfusion dynamics assessment with Power Doppler ultrasound in skeletal muscle during maximal and submaximal cycling exercise. Eur J Appl Physiol 118, 1209–1219 (2018). https://doi.org/10.1007/s00421-018-3850-y
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DOI: https://doi.org/10.1007/s00421-018-3850-y