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1 848 J. Physiol. (1963), 168, pp With 4 text-ftgurem Printed in Great Britain BLOOD FLOW AND VNOUS OXYGN SATURATION DURING SUSTAIND CONTRACTION OF TH FORARM MUSCLS BY H. BARCROFT, B. GRNWOOD AND R. F. WHLAN From the Sherrington School of Physiology, St Thomas's Hospital Medical School, London, S.. 1 (Received 1 December 1962) Barcroft & Millen (1939) found that blood flow in the muscles of the calf of the leg was probably arrested during strong contraction. On the other hand Grant (1938) and Humphreys & Lind (1962) found that in the forearm strong contraction was accompanied by increase in flow. The effects of contraction of the forearm muscles on forearm blood flow have been re-examined and the results described in this paper. Although the changes in venous blood oxygen saturation during rhythmic exercises of the legs have been carefully studied (Donald, Bishop & Wade, 1954; Donald, Bishop, Cumming & Wade, 1955; Donald, Wormald, Taylor & Bishop, 1957; Carlson & Pernow, 1961) and in the forearm (M6nod, Saint-Saens, Scherrer & Soula, 1961), the changes that accompany sustained contraction have received but little attention. Love (1955) studied the changes following relaxation, and reported the results of a few observations made during contraction. A further aim of our work was to record venous blood oxygen changes accompanying sustained contractions of different strengths. Most of the forearm muscles were involved in the exercises performed by our subjects. MTHODS The subjects were ourselves, our colleagues and volunteer medical students who lay supine on a couch in a laboratory maintained at C. A polythene catheter was inserted through a 17-gauge needle into an appropriate vein in the antecubital fossa or one arm and manipulated into the deep branch, being passed distally a distance of 3-5 cm into the muscles of the forearm (Mottram, 1955). Samples of blood withdrawn from a catheter so placed have been shown to come from the muscles (Roddie, Shepherd & Whelan, 1956; Coles, Cooper, Mottram & Occleshaw, 1958; Skinner & Whelan, 1962). In a number of experiments a second catheter was inserted into a superficial vein draining the skin of the forearm. The catheters were connected to a syringe containing heparin (1 u./ml.) in saline and kept free of blood between sampling periods by occasional flushing with a small amount of this solution. Water-filled plethysmographs were then applied to both forearms and maintained at a temperature of C throughout the experiment. Blood-flow records were obtained at 3 sec intervals during control periods and more frequently during and immediately following periods of forearm exercise.
2 BLOOD FLOW AND VNOUS OXYGN 849 Blood samples of 1 ml. were withdrawn anaerobically as required into nylon syringes, haemolysed immediately with saponin solution, and the blood oxygen saturation determined by the spectro-photometric technique described by Roddie, Shepherd & Whelan (1957). Blood-flow records and blood samples were taken alternately and care was taken to ensure that there was no venous congestion of the arm while samples were being withdrawn, in order to prevent contamination of the muscle blood with that from skin (Roddie et al. 1956). ~. 4 o In I..W L. o 1! 2 1 I 3 I v ui X _I c 12 Ls ;-2 Oc tō # Minutes Fig. 1. Results showing the effect of 3 strong, 3 moderate and 3 weak sustained contractions of the forearm muscles (shaded rectangles) on the oxygen saturation of the venous blood draining from the forearm muscles (solid squares); and on the blood flow in the exercised forearm (solid circles) and in the opposite resting forearm (open circles). xercise of the forearm muscles was carried out by squeezing with the hand a rubber bulb filled with water and connected to a glass tube of 1 cm internal diameter and 15 cm long, mounted vertically in view of the subject. The effects of strong, moderate and weak contractions were studied. To perform a strong contraction the subject squeezed the bulb as hard as he possibly could for 1 min. During the exercise the subject was repeatedly encouraged to keep squeezing as hard as he could. To perform a moderate contraction he raised the water level in the tube to a mark at 1 cm and kept it there for 4-5 min. Towards the end of this exercise he was encouraged not to give up. To perform the weak contraction he raised the water in the tube to a mark at 4 cm. where he could keep it without any difficulty for 1 min. He was then told to relax.
3 85 H. BARCROFT, B. GRNWOOD AND R. F. WHLAN RSULTS Blood flow. Results were obtained on the effects of strong contraction in 6 experiments, each on a different subject; on the effects of moderate contraction in 1 experiments, each on a different subject, and on the effects of weak contractions in 9 experiments, each on a different subject. 1 ; 5 c t o 24W._ 8 Q '.8 I- 'v I%- ou_ 1 -.-O c 14 C o "- 2 c- 'I 1 Minutes Fig. 2. Results showing the effect of strong and moderate sustained contractions of the forearm muscles (shaded rectangles) performed with normal circulation (left) and during occlusion of the brachial artery (right-stippled rectangles). Symbols as in Fig. 1. Typical changes are seen in Figs. 1 and 2. The results in each experiment are summarized in Fig. 3. Figure 4 shows the averaged results. The averaged blood flows before and at the end of the exercises just before relaxation are shown in Table 1. Deep venous oxygen saturation. Results were obtained in all the experiments already detailed and in addition on the effects of strong contraction in 4 more experiments on 3 more subjects. The effect of the contractions on venous oxygen saturation are shown in Figs The averaged oxygen saturations before exercise and the averaged lowest saturations at the end of the exercises, just before or after relaxation, are shown in Table 2.
4 BLOOD FLOW AND VNOUS OXYGN 851 TABL 1 Averaged blood flow and range (ml./1 ml. forearm/min) Before At end of Contraction exercise exercise Strong 4 (2-6) 14 (9-2) Medium 3 (2-7) 12 (6-2) Weak 3 (2-6) 11 (4-2) Strong Moderate Weak._ 2 - o - uw - (U Rest X 4X Rest X s Rest..X 1 Strong Moderate Weak C._ U 5 Rs. Rest ) c Rest X Fig. 3. Changes in forearm blood flow and in deep venous oxygen saturation caused by sustained contraction (X) of the forearm muscles with free circulation (@) and during digital occlusion of the brachial artery (). Rest X
5 852 H. BARCROFT, B. GRNWOOD AND R. F. WHLAN Oxygen consumption. Average figures are shown in Fig. 4. They have been calculated from the corresponding values for deep vein oxygen saturation and forearm blood flow. Arterial oxygen saturation was assumed to have been 2 vols. %. Muscle blood flow was obtained by Contraction Strong Medium Weak TABL 2 Averaged oxygen saturation (%) and range Lowest saturation Before at end of exercise exercises 54 (45-65) 27 (3-41) 49 (38-65) 34 (25-38) 46 (36-65) 44 (28-66) o c_ c 'o -- 2 D o O- C o LL K r- 4 8 g 3 -_6 -I -4 = \4 2 c c.- O X rc o -- u- 2 O Minutes Fig. 4. Averaged results showing the effect of strong (@) (1 min), moderate () (5 min) and weak (A) (1 min) sustained contraction of the forearm muscles, forearm blood flow, venous oxygen saturation, and oxygen uptake.
6 BLOOD FLOW AND VNOUS OXYGN 853 subtracting 1 ml. from forearm blood flow. Cooper, dholm & Mottram (1954) found that muscle flow accounts for 3 ml. out of a resting flow of 4 ml. The subtraction of 1 ml. during exercise is probably justified, since skin flow is likely to be reduced and to form a relatively smaller fraction of total forearm flow. Superficial venous oxygen saturation was determined in a few experiments and decreased during exercise, because of constriction in the skin, or shunting of blood from deep to superficial veins, as reported by Cooper, Randall & Hertzman (1959). DISCUSSION The forearm was chosen for recording venous blood oxygen changes accompanying sustained contraction because it was highly desirable that the samples of venous blood used for the oxygen estimations should be taken from veins draining the active muscles. Contamination with blood from the hand can be avoided by arresting the circulation to this part. Contamination with blood from the overlying skin is easily avoided in the forearm, because a catheter can be passed retrogradely into one of the deep veins (Mottram, 1955), a procedure it would probably be unwise to attempt in the leg where damage to the venous valves might have unpleasant results. Grant (1938) and Humphreys & Lind (1962) found that forearm blood flow increased during strong sustained contraction of the forearm muscles. On the other hand Barcroft & Millen (1939) concluded that blood flow in the calf of the leg must be arrested during tip-toe standing. This was thought to be due to mechanical compression of the vessels. These contrasting effects of strong contraction on blood flow in the forearm and in the calf may have an anatomical explanation. Strong contraction of the calf muscles may nip their arteries; in the forearm this may not happen. In the forearm, as Fig. 4 shows, the greater the strength of contraction the more rapid was the rise in blood flow. Blood flow at the end of strong contractions was a little greater than that at the end of moderate contractions; but this difference might not be seen in the results ofa larger series of experiments. During weak contractions hyperaemia developed more gradually and at the end of the contraction it was a little less than that at the end of moderate and strong contractions. Relaxation of strong and moderate contractions was accompanied by a large and abrupt increase in flow, no doubt due to the sudden cessation of mechanical restriction. The peak flows after strong and moderate contractions were about the same, but the flow subsided a little more quickly after the strong contractions. This may have been because their duration was shorter. The rise in flow after weak contractions was inconspicuous, no doubt because mechanical restriction was quite small.
7 854 H. BARCROFT, B. GRNWOOD AND R. F. WHLAN To turn now to the oxygen saturations. Love (1955) found that oxygen saturation usually decreased but sometimes increased during sustained contraction, results like those we obtained during weak contractions. In our experiments, as Fig. 4 shows, the stronger the contraction the greater was the decrease in oxygen saturation-and the greater the mechanical restriction of the blood flow. If there had been no mechanical hindrance to flow there might have been no change in venous oxygen saturation. We cannot tell. On the other hand, one might suppose that strongly contracting muscles could desaturate the blood completely. Yet we see that at the end of such contraction the blood was often 25 % saturated. In only one case, with free circulation, did the blood become almost fully desaturated. If the arterial supply to muscle is restricted by occlusion of the brachial artery, desaturation is in fact nearly complete. This is seen in Fig. 2 in the right-hand diagrams. Oxygen saturation decreased to 6 % at the end of a strong contraction and to 8 % at the end of a moderate one. Since active muscle can desaturate blood almost completely we come back to the question of why in the limb with unoccluded brachial artery did strong contraction commonly desaturate the blood to about 25 %. Can it have been that our samples from the deep forearm veins were really mixtures of desaturated blood from the active muscles and highly saturated blood from elsewhere? This seems unlikely, since the saturation of the blood draining from the isolated dog's gastrocnemius muscle was still around 25 % during maximum tetanic stimulation (Kramer & Quensel, 1937; Quensel & Kramer, 1939). It is more reasonable to suppose that for reasons we cannot explain contracting human muscle, supplied with normal vessels, cannot desaturate blood completely during strong sustained effort. After strong and moderate exercise, as Fig. 4 shows, oxygen saturation rose above the resting level, as has been fdund by Love (1955), and as can be seen in some of the tracings from the experiment of Kramer et al. (1937) on the dog's isolated gastrocnemius. Why this should be so is not known. According to Abramson & Ferris (194) skeletal muscle accounts for about 6 % of the segment of the forearm enclosed in the plethysmograph. We have used this figure, and those we have given for forearm blood flow and for venous oxygen saturation, to calculate average muscle oxygen uptakes. It must be emphasized that in individual experiments these would differ widely. Average resting oxygen uptake was *5 ml./ml. muscle, as compared with -28 found by Mottram; the difference is probably because our muscles had not been rested for so long. Average oxygen consumption just before relaxing a strong contraction was *3 ml./ml. muscle/min, a sixfold increase.
8 BLOOD FLOW AND VNOUS OXYGN 855 SUMMARY 1. The exercise used was squeezing a bulb; it was chosen so as to involve most of the forearm muscles. 2. Forearm blood flow was determined by venous occlusion plethysmography. 3. The blood samples used for oxygen estimations were taken from a catheter lying in a deep forearm vein. The circulation through the hand was arrested while sampling. 4. Mean forearm blood flows, before and at the end of exercise were: Strong contraction 4 > 14 ml./1 ml. forearm/min Moderate contraction 3 > 12 ml./1 ml. forearm/min Weak contraction 3 o- 11 ml./1 ml. forearm/min 5. Mean venous blood saturation, before and at the end of exercise were: Strong contraction (1 min) 54 > 27% Moderate contraction (4-5 min) % Weak contraction (1 min) 48 > 44 % The fall in oxygen saturation was related to the strength of contraction. 6. Increase in oxygen uptake during strong and moderate contractions was mediated by increase in utilization and blood flow, but predominantly by increase in blood flow during weak contraction. We are indebted to those students who volunteered as subjects, to Dr J. Silver for his assistance with many of the experiments, and to Mr Peter Dear for technical assistance. RFRNCS ABRAMSON, D. I. & FRRIs,. B. (194). Responses of blood vessels in the resting hand and forearm to various stimuli. Amer. Heart J. 19, BARCROFT, H. & MILLN, J. L.. (1939). The blood flow through muscle during sustained contraction. J. Phy8iol. 97, CARLSON, L. S. & PRNOW, B. (1961). Studies on the peripheral circulation and metabolism in man. Acta physiol. 8cand. 52, COLS, D. R., COOPR, K.., MOTTRAM, R. F. & OCCLSHAW, J. V. (1958). The source of blood samples withdrawn from deep forearm veins via catheters passed upstream from the median cubital vein. J. Phy8iol. 142, COOPR, K.., DHOLM,. G. & MOTTRAM, R. F. (1954). The partition of the blood between skin and muscle in the human forearm. J. Phy8iol. 123, 33P. COOPR, T., RANDALL, T. C. & HRTZMANN, A. B. (1959). Vascular convection of heat from active muscle to overlying skin. J. appl. Phy8iol. 14, DONALD, K. W., BISHOP, J. M., CUMMING, G. & WAD,. L. (1955). The effect of exercise on the cardiac output and circulatory dynamics of normal subjects. Clin. Sci. 14, 37. DONALD, K. W., BISHOP, J. M. & WAD,. L. (1954). A study of minute to minute changes of arterio-venous oxygen content difference, oxygen uptake and cardiac output and rate of achievement of a steady state during exercise in rheumatic heart disease. J. clin. Invest. 33, DONALD, K. W., WORMALD, P. N., TAYLOR, S. H. & BISHOP, J. M. (1957). Changes in the oxygen content of femoral venous blood and leg blood flow during leg exercise in relation to cardiac output response. Clin. Sci. 16,
9 856 H. BARCROFT, B. GRNWOOD AND R. F. WHLAN GRANT, R. T. (1938). Observations on the blood circulation in voluntary muscle in nman. Clin. Sci. 3, HUMPHRYS, P. W. & LIND, A. R. (1963). Blood flow through active muscles of the forearm during sustained hand-grip contractions. J. Physiol. 163, 18P. KRAMR, K. & QUNSL, W. (1937). Untersuchungen uber den Muskelstoffwechsel des Warmbluters. I. Mitteilung. Der Verlauf der Muskeldurchblutung wahrend der tetanischen Kontraktion. Pflug. Arch. ges. Physiol. 239, 621. LOV, A. H. G. (1955). The rate of blood flow and the oxygen saturation of the effluent blood following contraction of the muscles of the human forearm. Clin. Sci. 14, MONOD, H., SAINT-SAXS, M., SCHRRR, J. & SOULA, C. (1961). etudes du travail musculaire et de la fatigue. III. Le sang veineux efferent d'un muscle effectuant un travail dynamique chez l'homme. J. Physiol., Paris, 53, MOTTRAM, R. F. (1955). Oxygen consumption of human skeletal muscle in vivo. J. Physiol. 128, QUNSL, W. & KRAMR, K. (1939). Untersuchungen uber den Muskelstoffwechsel des Warmbluters. II. Mitteilung. Die Sauerstoffrafnahme des Muskels wahrend der tetanischen Kontraktion. Pflug. Arch. ges. Physiol. 241, 698. RODDI, I. C., SHPHRD, J. T. & WHLAN, R. F. (1956). vidence from venous oxygen saturation measurements that the increase in forearm blood flow during body heating is confined to the skin. J. Physiol. 134, RODDI, I. C., SHPHRD, J. T. & WHLAN, R. F. (1957). A spectrophotometric method for the rapid estimation of blood oxygen saturation, content and capacity. J. clin. Path. 1, SKINNR, S. L. & WHLAN, R. F. (1962). The circulation in forearm skin and muscle during adrenaline infusions. Aust. J. exp. biol. Sci. 4,
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