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Limb and skeletal muscle blood flow measurements at rest and during exercise in human subjects

Published online by Cambridge University Press:  12 June 2007

Göran Rådegran
Göran Rådegran*
Affiliation:
Copenhagen Muscle Research Centre, Rigshospitalet, Section 7652, Tagensvej 20, Dk-2200 Copenhagen N, Denmark
*
Corresponding Author: Göran Rådegran, fax +45 3545 7634, email [email protected]
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Abstract

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The aim of the present review is to present techniques used for measuring blood flow in human subjects and advice as to when they may be applicable. Since blood flow is required to estimate substrate fluxes, energy turnover and metabolic rate of skeletal muscle, accurate measurements of blood flow are of extreme importance. Several techniques have therefore been developed to enable estimates to be made of the arterial inflow to, venous outflow from, or local blood flow within the muscle. Regional measurements have been performed using electromagnetic flow meters, plethysmography, indicator methods (e.g. thermodilution and indo-cyanine green dye infusion), ultrasound Doppler, and magnetic resonance velocity imaging. Local estimates have been made using 133Xe clearance, microdialysis, near i.r. spectroscopy, positron emission tomography and laser Doppler. In principle, the aim of the study, the type of interventions and the limitations of each technique determine which method may be most appropriate. Ultrasound Doppler and continuous indo-cyanine green dye infusion gives the most accurate limb blood flow measurements at rest. Moreover, the ultrasound Doppler is unique, as it does not demand a steady-state, and because its high temporal resolution allows detection of normal physiological variations as well as continuous measurements during transitional states such as at onset of and in recovery from exercise. During steady-state exercise thermodilution can be used in addition to indo-cyanine green dye infusion and ultrasound Doppler, where the latter is restricted to exercise modes with a fixed vessel position. Magnetic resonance velocity imaging may in addition be used to determine blood flow within deep single vessels. Positron emission tomography seems to be the most promising tool for local skeletal muscle blood-flow measurements in relation to metabolic activity, although the mode and intensity of exercise will be restricted by the apparatus design.

Keywords

Blood flowExerciseMuscle metabolismHyperaemia
Type
Meeting Report
Information
Proceedings of the Nutrition Society , Volume 58 , Issue 4 , November 1999 , pp. 887 - 898
Copyright
The Nutrition Society

References

Andersen, P & Saltin, B (1985) Maximal perfusion of skeletal muscle in man. Journal of Physiology 366, 233–249.CrossRefGoogle ScholarPubMed
Barcroft, H & Dornhorst, AC (1949) The blood flow through the human calf during rhythmic exercise. Journal of Physiology 109, 402–411.CrossRefGoogle ScholarPubMed
Benjamin, N, Calver, A, Collier, J, Robinson, B, Vallance, P & Webb, D (1995) Measuring forearm blood flow and interpreting the responses to drugs and mediators. Hypertension 25, 918–923.CrossRefGoogle ScholarPubMed
Bonde-Petersen, F, Henriksson, J & Lundin, B (1975) Blood flow in thigh muscle during bicycling exercise at varying work rates. European Journal of Applied Physiology 34, 191–197.CrossRefGoogle ScholarPubMed
Bonde-Petersen, F & Siggaard-Andersen, J (1967) Blood flow in skin and muscle, evaluated by simultaneous venous occlusion plethysmography and 133Xe clearance. Scandinavian Journal of Clinical and Laboratory Investigation 19, 113–119.CrossRefGoogle Scholar
Bonde-Petersen, F & Siggaard-Andersen, J (1969) Simultaneous venous occlusion plethysmography and 133Xe clearance in patients with arteriosclerosis of the lower extremities. An attempt to evaluate the blood flow in skin and muscle. Scandinavian Journal of Thoracic Cardiovascular Surgery 3, 20–25.CrossRefGoogle Scholar
Boushel, R, Ide, K, Møller-Sørensen, H, Fernandes, A, Pott, F & Secher, N (1997) Muscle microvascular blood flow during exercise determined by near infrared spectroscopy. Journal of Biomedical Optics 1, 145–149.Google Scholar
Brodie, TG & Russell, AE (1905) On the determination of the rate of blood-flow through an organ. Journal of Physiology 32, 47–49.Google Scholar
Bygdeman, S & Pernow, B (1978) Venös ocklutionspletysmografi (Venous occlusion plethysmography). In Perifer Cirkulation. Kliniska Fysiologiska Undersökningsmetoder (Peripheral Circulation. Clinical Physiological Investigation Methods), pp. 61–74 [Pernow, B, editor]. Stockholm: AWE Gebers.Google Scholar
Byström, S, Jensen, B, Jensen-Urstad, M, Lindblad, LE & Kilbom, A (1998) Ultrasound-Doppler technique for monitoring blood flow in the brachial artery compared with occlusion plethysmography of the forearm. Scandinavian Journal of Clinical and Laboratory Investigation 58, 569–576.CrossRefGoogle ScholarPubMed
Cerretelli, P, Marconi, C, Pendergast, D, Meyer, M, Heisler, N & Piiper, J (1984) Blood flow in exercising muscles by xenon clearance and by microsphere trapping. Journal of Applied Physiology 56, 24–30.CrossRefGoogle ScholarPubMed
Chapman, JV (1990) The technical aspects of Doppler ultrasound. In The Noninvasive Evaluation of Hemodynamics in Congenital Heart Disease, pp. 1–34 [Chapman, JV and Sutherland, Gr, editors.] London: Kluwer Academic Publisher.CrossRefGoogle Scholar
Choi, Y, Huang, SC, Hawkins, RA, Kuhle, WG, Dahlbom, M, Hoh, CK, Czernin, J, Phelps, ME & Schelbert, HR (1993) A simplified method for quantification of myocardial blood flow using nitrogen-13-ammonia and dynamic PET. Journal of Nuclear Medicine 34, 488–497.Google ScholarPubMed
Clausen, JP & Lassen, NA (1971) Muscle blood flow during exercise in normal man studied by the 133-xenon clearance method. Cardiovascular Research 5, 245–254.CrossRefGoogle Scholar
Conrad, MC & Green, HD (1961) Evaluation of venous occlusion plethysmography. Journal of Applied Physiology 16, 289–292.CrossRefGoogle Scholar
Cronestrand, R (1970) Leg blood flow at rest and during exercise after reconstruction for occlusive disease. Scandinavian Journal of Thoracic Cardiovascular Surgery, Suppl. 4, 1–24.CrossRefGoogle ScholarPubMed
De Blasi, RA, Ferrari, M, Natali, A, Conti, G, Mega, A & Gasparetto, A (1994) Noninvasive measurement of forearm blood flow and oxygen consumption by near-infrared spectroscopy. Journal of Applied Physiology 76, 1388–1393.CrossRefGoogle ScholarPubMed
Djordjevich, L & Sadove, MS (1981) Basic principles of electrohaemodynamics. Journal of Biomedical Engineering 3, 25–33.CrossRefGoogle ScholarPubMed
Edler, I & Hertz, CH (1954) Use of ultrasonic reflectoscope for continuous recording of movements of heart wall. Kungliga Fysiografiska Sällskapet 24, 40–58.Google Scholar
Edwards, AD, Richardson, C, van der, Zee P, Elwell, C, Wyatt, JS, Cope, M, Delpy, DT & Reynolds, EOR (1993) Measurement of hemoglobin flow and blood flow by near infrared spectroscopy. Journal of Applied Physiology 75, 1884–1889.CrossRefGoogle ScholarPubMed
Enzmann, DR, Marks, MP & Pelc, NJ (1993) Comparison of cerebral artery blood flow measurements with gated cine and ungated phase-contrast techniques. Journal of Magnetic Resonance Imaging 3, 705–712.CrossRefGoogle ScholarPubMed
Eriksen, M (1992) Effects of pulsatile arterial diameter variations on blood flow estimated by Doppler Ultrasound. Medical and Biological Engineering and Computation 30, 46–50.CrossRefGoogle ScholarPubMed
Fegler, G (1954) Measurement of cardiac output in anaesthethized animals by a thermo-dilution method. Quarterly Journal of Experimental Physiology 39, 153–164.CrossRefGoogle Scholar
Firmin, DN, Nayler, GL, Klipstein, RH, Underwood, SR, Rees, RSO. & Longmore, DB (1987) In vivo validation of MR velocity imaging. Journal of Computer Assisted Tomography 11, 751–756.CrossRefGoogle ScholarPubMed
Fronek, A & Ganz, V (1960) Measurement of flow in single blood vessels including cardiac output by local thermodilution. Circulation Research 8, 175–182.CrossRefGoogle Scholar
Ganz, V, Hlavová, A, Fronek, A, Linhart, J & Prerovsky, I (1964) Measurement of blood flow in the femoral artery in man at rest and during exercise by local thermodilution. Circulation 30, 86–89.CrossRefGoogle Scholar
Ganz, W & Swan, HJC (1974) Measurement of blood flow by the thermodilution technique. In The Theory and Practice of Indicator Dilution, pp. 245–266 [Bloomfield, DA, editor.] Baltimore, MD: University Park Press.Google Scholar
Gill, RW (1979) Pulsed doppler with b-mode imaging for quantitative blood flow measurement. Ultrasound in Medicine and Biology 5, 223–235.CrossRefGoogle ScholarPubMed
Gill, RW (1985) Measurement of blood flow by ultrasound: accuracy and sources of error. Ultrasound in Medicine and Biology 11, 625–641.CrossRefGoogle ScholarPubMed
Gonzales, JA, Calbet, JAL & Nielsen, B (1998) Muscle blood flow is reduced with dehydration during prolonged exercise in humans. Journal of Physiology 513, 895–905.CrossRefGoogle Scholar
Grimby, G, Häggendahl, E & Saltin, B (1967) Local 133xenon clearance from the quadriceps muscle during exercise in man. Journal of Applied Physiology 22, 305–310.CrossRefGoogle Scholar
Hall, KV (1969) Postoperative blood flow measurements in man by the use of implanted electromagnetic probes. Scandinavian Journal of Thoracic Cardiovascular Surgery 3, 135–144.CrossRefGoogle Scholar
Herscovitch, P, Markham, J & Raichle, ME (1983) Brain blood flow measured with intravenous H215O. I. Theory and error analysis. Journal of Nuclear Medicine 24, 782–789.Google ScholarPubMed
Hewlett, AW & van Zwaluwenburg, JG (1909) The rate of blood flow in the arm. Heart 1, 87–97.Google Scholar
Hickner, RC, Bone, D, Ungerstedt, U, Jorfeldt, L & Henriksson, J (1994a) Muscle blood flow during intermittent exercise: comparison of the microdialysis ethanol technique and 133Xe clearance. Clinical Science 86, 15–25.CrossRefGoogle ScholarPubMed
Hickner, RC, Ekelund, U, Mellander, S, Ungerstedt, U & Henriksson, J (1995) Muscle blood flow in cats: comparison of microdialysis ethanol technique with direct measurement. Journal of Applied Physiology 79, 638–647.CrossRefGoogle ScholarPubMed
Hickner, RC, Rosdahl, H, Borg, I, Ungerstedt, U, Jorfeldt, L & Henriksson, J (1991) Ethanol may be used with the microdialysis technique to monitor blood flow changes in skeletal muscle: dialysate glucose concentration is blood-flow-dependent. Acta Physiologica Scandinavica 143, 355–356.CrossRefGoogle ScholarPubMed
Hickner, RC, Rosdahl, H, Borg, I, Ungerstedt, U, Jorfeldt, L & Henriksson, J (1992) The ethanol technique of monitoring local blood flow changes in rat skeletal muscle: implications for microdialysis. Acta Physiologica Scandinavica 146, 87–97.CrossRefGoogle ScholarPubMed
Hickner, RC, Ungerstedt, U & Henriksson, J (1994b) Regulation of skeletal muscle blood flow during acute insulin-induced hypoglycemia in the rat. Diabetes 43, 1340–1344.CrossRefGoogle ScholarPubMed
Holloway, GA & Watkins, DW (1977) Laser Doppler measurements of cutaneous blood flow. Journal of Investigative Dermatology 69, 306–309.CrossRefGoogle ScholarPubMed
Howry, DH & Bliss, WR (1952) Ultrasonic visualization of soft tissue structures in the body. Journal of Laboratory and Clinical Medicine 40, 579–592.Google Scholar
Hundley, WG, Lange, RA, Clarke, GD, Meshack, BM, Payne, J, Landau, C, McColl, R, Sayad, DE, Willet, DW, Willard, JE, Hillis, LD & Peshock, RM (1996) Assessment of coronary flow and flow reserve in humans with magnetic resonance imaging. Circulation 93, 1502–1508.CrossRefGoogle ScholarPubMed
Jensen, BR, Sjøgaard, G, Bornmyr, S, Arborelius, M & Jørgensen, K (1995) Intramuscular laser-Doppler flowmetry in the supraspinatus muscle during isometric contractions. European Journal of Applied Physiology 71, 373–378.CrossRefGoogle ScholarPubMed
Jorfeldt, L, Juhlin-Dannfelt, A, Pernow, B & Wassén, E (1978) Determination of human leg blood flow: a thermodilution technique based on femoral venous bolus injection. Clinical Science and Molecular Medicine 54, 517–523.Google ScholarPubMed
Jorfeldt, L & Wahren, J (1971) Leg blood flow during exercise in man. Clinical Science 41, 459–473.CrossRefGoogle ScholarPubMed
Keidel, WD (1950) Über eine methode zur repiestrierig der volumanderung des herzens am menschen (A new method for recording volume changes of the heart in man). Zeitschrift für Kreislaufforschung 39, 257–271.Google Scholar
Kety, S (1951) The theory and applications of the exchange of inert gas at the lung and tissues. Pharmacology Review 3, 1–41.Google Scholar
Kolin, A (1936) An electromagnetic flowmeter. Principle of the method and its application to blood flow measurements. Proceedings of the Society for Experimental of Biology and Medicine 35, 53–56.CrossRefGoogle Scholar
Kolin, A (1941) An A.C. induction flow meter for measurement of blood flow in intact blood vessels. Proceedings of the Society for Experimental Biology and Medicine 46, 235–239.CrossRefGoogle Scholar
Lassen, NA, Henriksen, O & Sejrsen, P (1983) Indicator methods for measurement of organ and tissue blood flow. In Handbook of Physiology. Section 2, The Cardiovascular System: Peripheral Circulation and Organ Blood Flow, Vol. 3, part 1, pp. 21–63 [JT, Shepherd, FM, Abboud and SR, Geiger, editors. Bethesda, MD: American Physiology Society.Google Scholar
Lassen, NA, Linbjerg, I & Munck, O (1964) Measurement of blood flow through skeletal muscle by intramuscular injection of xenon 133. Lancet i, 686–689.CrossRefGoogle Scholar
Li, H, Clarke, GD, NessAvier, M, Liu, H & Peshock, R (1995) Magnetic resonance imaging k-space segmentation using phase-encoding groups: The accuracy of quantitative measurements of pulsatile flow. Medical Physics 22, 391–399.CrossRefGoogle Scholar
McCauley, TR, Pena, CS, Holland, CK, Price, TB & Gore, JC (1995) Validation of volume flow measurements with cine phase-contrast MR imaging for peripheral arterial waveforms. Journal of Magnetic Resonance Imaging 5, 663–668.CrossRefGoogle ScholarPubMed
Muzik, O, Beanlands, RSB, Hutchins, GD, Mangner, TJ, Nguyen, N & Schwaiger, M (1993) Validation of nitrogen-13-ammonia tracer kinetic model for quantification of myocardial blood flow using PET. Journal of Nuclear Medicine 34, 83–91.Google ScholarPubMed
Rådegran, G (1997) Ultrasound Doppler estimates of femoral artery blood flow during dynamic knee extensor exercise in humans. Journal of Applied Physiology 83, 1383–1388.CrossRefGoogle ScholarPubMed
Rådegran, G, Pilegaard, H, Nielsen, JJ & Bangsbo, J (1998) Microdialysis ethanol removal reflects probe recovery rather than local blood flow in skeletal muscle. Journal of Applied Physiology 85, 751–757.CrossRefGoogle ScholarPubMed
Rådegran, G & Saltin, B (1998) Muscle blood flow at onset of dynamic exercise in humans. American Journal of Physiology 274, H314–H322.Google ScholarPubMed
Rådegran, G & Saltin, B (1999) Nitric oxide in the regulation of vasomotor tone in human skeletal muscle. American Journal of Physiology 276, H1951–H1960.Google ScholarPubMed
Raichle, ME, Martin, WRW, Herscovitch, P, Mintun, MA & Markham, J (1983) Brain blood flow measured with intravenous H215O. II. Implementation and validation. Journal of Nuclear Medicine 24, 790–798.Google ScholarPubMed
Raitakari, M (1996) Muscle blood flow and insulin sensitivity. Doctoral Thesis, Turku PET Center and the Department of Medicine and Nuclear Medicine, Turku, Finland.Google Scholar
Raitakari, M, Nuutila, P, Ruotsalainen, U, Teräs, M, Eronen, E, Laine, H, Raitakari, OT, Iida, H, Knuuti, MJ & Yki-Järvinen, H (1996) Relationship between limb and muscle blood flow in man. Journal of Physiology 496, 543–549.CrossRefGoogle ScholarPubMed
Rosdahl, H, Ungerstedt, U, Jorfeldt, L & Henriksson, J (1993) Interstitial glucose and lactate balance in human skeletal muscle and adipose tissue studied by microdialysis. Journal of Physiology 471, 637–657.CrossRefGoogle ScholarPubMed
Rowell, LB (1993) Human Cardiovascular Control. Oxford: Oxford University Press.CrossRefGoogle Scholar
Ruotsalainen, U, Raitakari, M, Nuutila, P, Oikonen, V, Sipilä, H, Teräs, M, Knuuti, J, Bloomfield, PM & Iida, H (1997) Quantitative blood flow measurement of skeletal muscle using oxygen-15-water and PET. Journal of Nuclear Medicine 38, 314–319.Google ScholarPubMed
Saltin, B (1985) Hemodynamic adaptions to exercise. American Journal of Cardiology 55, 42D–47D.CrossRefGoogle ScholarPubMed
Saltin, B & Gollnick, PD (1983) Skeletal muscle adaptability: significance for metabolism and performance. In Handbook of Physiology. Skeletal Muscle, pp. 555–631 [Peachey, LD, Adrian, RH and Geiger, SR, editors.] Bethesda, MD: American Physiology Society.Google Scholar
Saltin, B & Rowell, LB (1980) Functional adaptions to physical activity and inactivity. Federation Proceedings 39, 1506–1513.Google ScholarPubMed
Satamura, S & Kaneko, Z (1960) Ultrasonic rheograph. Proceedings from the International Conference on Medical Electronics 3, 239–242.Google Scholar
Schäfer, EA & Moore, B (1896) On the contractility and inervation of the spleen. Journal of Physiology 20, 1–51.CrossRefGoogle Scholar
Shoemaker, JK, Pozeg, ZI & Hughson, RL (1996) Forearm blood flow by Doppler ultrasound during rest and exercise: test of day-to-day repeatability. Medicine and Science in Sports and Exercise 28, 1144–1149.CrossRefGoogle ScholarPubMed
Siggaard-Andersen, J (1970) Venous occlusion plethysmograph on the calf. Doctoral Thesis. University of Copenhagen, Denmark.Google Scholar
Siggaard-Andersen, J & Bonde-Petersen, F (1967) Venous occlusion plethsmography and 133Xe muscle clearance measured simultaneously on the calf in normal subjects. Scandinavian Journal of Clinical and Laboratory Investigation 19, 106–112.CrossRefGoogle Scholar
Sørlie, D & Myhre, K (1977) Determination of lower leg blood flow in man by thermodilution. Scandinavian Journal of Clinical and Laboratory Investigation 37, 117–124.CrossRefGoogle Scholar
Stallknecht, B, Donsmark, M, Enevoldsen, LH, Fluckey, JD & Galbo, H (1999) Estimation of rat muscle blood flow by microdialysis probes perfused with ethanol, [14C\ethanol, and 3H2O. Journal of Applied Physiology 86, 1054–1061.CrossRefGoogle ScholarPubMed
Stewart, GN (1897) Researches on the circulation time and on the influences which affect it. IV. The output of the heart. Journal of Physiology 22, 159–183.CrossRefGoogle Scholar
Stewart, GN (1921) The pulmonary circulation time, the quantity of blood in the lungs and the output of the heart. American Journal of Physiology 58, 20–44.CrossRefGoogle Scholar
Tønnesen, KH (1964) Blood flow through muscle during rhythmic contraction measured by xenon. Scandinavian Journal of Clinical and Laboratory Investigation 16, 646–654.CrossRefGoogle ScholarPubMed
Tønnesen, KH & Sejrsen, P (1970) Washout of 133Xenon after intramuscular injection and direct measurement of blood flow in skeletal muscle. Scandinavian Journal of Clinical and Laboratory Investigation 25, 71–81.CrossRefGoogle ScholarPubMed
Vallé, JPM, Sostman, HD, MacFall, JR, DeGrado, TR, Zhang, J, Sebbag, L, Cobb, FR, Wheeler, T, Hedlund, LW, Turkington, TG, Spritzer, CE & Coleman, RE (1998) Quantification of myocardial perfusion by MRI after coronary occlusion. Magnetic Resonance in Medicine 40, 287–297.CrossRefGoogle Scholar
Vänttinen, E (1975) Electromagnetic measurement of the arterial blood flow in the femeropopliteal region. Acta Chirurgica Scandinavica 141, 353–359.Google Scholar
Wahren, J & Jorfeldt, L (1973) Determination of leg blood flow during exercise in man: an indicator-dilution technique based on femoral venous dye infusion. Clinical Science and Molecular Medicine 45, 135–146.Google Scholar
Wallgren, F, Amberg, G, Hickner, RC, Ekelund, U, Jorfeldt, L & Henriksson, J (1995) A mathematical model for measuring blood flow in skeletal muscle with the microdialysis ethanol technique. Journal of Applied Physiology 79, 648–659.CrossRefGoogle ScholarPubMed
Walløe, L & Wesche, J (1988) Time course and magnitude of blood flow changes in the human quadriceps muscles during and following rhythmic exercise. Journal of Physiology 405, 257–273.CrossRefGoogle ScholarPubMed
Webster, JG (1978) Medical Instrumentation – Application and Design.Boston, MA: Houghton Mifflin Company.CrossRefGoogle Scholar
Wesche, J (1986) The time course and magnitude of blood flow changes in the human quadriceps muscles following isometric contraction. Journal of Physiology 377, 445–462.CrossRefGoogle ScholarPubMed
Whitney, RJ (1953) The measurement of volume changes in human limbs. Journal of Physiology 121, 1–27.CrossRefGoogle ScholarPubMed
Wild, JJ & Neal, D (1951) Use of high frequency ultrasonic waves for detecting changes in texture in living tissues. Lancet i, 655.Google Scholar
Williams, CA & Lind, AR (1979) Measurement of forearm blood flow by venous occlusion plethysmography: influence of hand blood flow during sustained and intermittent isometric exercise. European Journal of Applied Physiology 42, 141–149.CrossRefGoogle ScholarPubMed
Zananiri, FV, Jackson, PC, Halliwell, M, Harris, RA, Hayward, JK, Davies, ER & Wells, PNT (1993) A comparative study of velocity measurements in major blood vessels using magnetic resonance imaging and Doppler ultrasound. British Journal of Radiology 66, 1128–1133.CrossRefGoogle ScholarPubMed