Arm blood flow at rest and during arm exercise G. AHLBORG Department
AND
M. JENSEN-URSTAD
of Clinical Physiology, Mdersjukhuset,
AHLBORG, G., AND M. JENSEN-URSTAD. Arm bloodflow at rest and during arm exercise. J. Appl. Physiol. 70(2): 928-933,
1991.-To test the applicability of a dye-dilution method to quantitate total arm blood flow at rest and during arm exercise, indocyanine green was infused at a constant rate into the brachial artery. Eight subjectsperformed continuous 30-min arm exerciseswith an increasein intensity every 10min (30,60, and 90 W). The loads correspondedto 29 t 1,48 k 2, and 78 t 4% (means 2 SE) of the maxima! O2uptake (vozmax 2.13 t 0.08 l/min) during arm exercise. Vozrnarduring arm exercise was 61 -+ 1.7% of that during leg exercise. The dye concentration was analyzed in blood samplesfrom three arm veins, two ipsiand one contralateral, at shoulder level. Corresponding dye concentrations in both ipsilateral veins and a stableconcentration difference between ipsi- and contralateral veins were achieved. Total arm blood flow wascalculated to be 0.21 t 0.04 l/min at rest and 2.43 k 0.14l/min at 90 W. Arm 0, uptake rose from 9 k 2 to 323 & 21 ml/min. Arm blood flow and 0, uptake each correlated linearly with both work load (r = 0.98) and pulmonary 0, uptake (r 2 0.98). Mechanical efficiency for the arm and body was 34-44 and 16-19%, respectively. We conclude that arm blood flow can be determined by continuous infusion of indocyanine green. indocyanine green;pulmonary oxygen uptake; arm oxygen UPtake; mechanicalefficiency
A SUITABLE METHOD for the determination of total arm blood flow is required for the study of arm hemodynamics and application of the Fick principle for quantitations of arm metabolism at rest and during arm exercise with muscles including those of the upper arm. No such method that is applicable both at rest and during exercise has been described before. Several methods are available for forearm or leg blood flow determinations. The venous occlusion meth .od has been used for forearm m.ainly when the a rm is at blood flow determinations rest. It has also been employed for determinations of calf blood flow during rhythmic exercise (4). During exercise,
The thermodilution principle, which has been used for determinations of femoral blood flow at rest as well as during exercise (2,8, 10,12), is probably less suitable for measuring arm blood flow . The method requires that the injection of indicator and temperature measurements be made in the same blood vessel. In this c ontext, the anatomy of the axillary artery and the fact that the axillary vein is not the only vein draining the arm present problems (Fig. 1). 928
0161-7567/91
$1.50
Copyright
S-l 00 64 Stockholm, Sweden
Dye-dilution methods can be designed to circumvent the disadvantages of the thermodilution methods. By application of a dye-dilution technique, the indicator can be infused intra-arterially and measurements can be performed in venous blood, thereby increasing the chances of uniform mixing of the indicator infused with the amount of blood flowing through the arm. Intra-arterial infusion of dye has been used to measure forearm blood flow at rest (3) and during different types of forearm exercises (11, 14, 15). In addition, a constant dye-infusion technique has been employed for measurements of total leg blood flow at rest and during exercise (13). The aim of the present study was to investigate whether it is possible, with the complex vascular system of the arm, to determine total arm blood flow at rest and during arm exercise by a constant infusion of dye into the brachial artery and postmix sampling in the axillary vein. METHODS
Subjects. Eight healthy male subjects were studied in the l2- to 14-h postabsorptive state. The subjects were physically active and well trained but did not participate in competitive athletics. Data on age, body dimensions, and maximal 0, uptake during leg and arm exercise are presented in Table 1. All subjects were informed of the nature, purpose, and possible risks involved in the study before they gave voluntary consent to participate. The procedures in these studies have been reviewed and approved by the institutional Ethics Committee. Procedure. Four thin Teflon catheters (1.0 mm ID, 1.4 mm OD, 600 mm lng) were inserted percutaneously. One catheter was introduced into the right brachial artery in the cubital region and directed 15-20 cm proximally. Another three catheters were inserted at the arm fold in two different arm veins of the ipsilateral arm and in one contralateral arm vein. The position of the ipsilateral venous catheter is of importance because of the possibility of an admixture of blood from vascular beds other than those of the arm. To estimate the influence of the catheter position on the dye concentration, two catheters (V, and V,) were introduced in different veins (V, in the median cubital vein, which is a superficial connection between the cephalic and the basilic vein, and V, in the basilic vein) at the ipsilateral arm fold and positioned up to 5 cm apart with their tips at the level of v. axillaris (Fig. 1). The distance (D) in centimeters from the point of introduction to the coracoid process was estimated so that the catheter could be positioned without fluoroscopic control. The V, tip was inserted at D or up to D + 3 cm. The V, tip was advanced 2-5 cm, but not more than D + 5 cm,
0 1991 the American
Physiological
Society
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ARM
BLOOD
FLOW
AT
REST
v.
FIG. 1. Anatomy of venous system of upper arm. [Adapted from Hafferl (8a) .]
beyond the V, tip. The tips of the ipsilateral catheters were assumed to be somewhere at the level of the confluence of the cephalic and the axillary vein (Fig. 1). To check the catheter positions, fluoroscopic controls were performed and revealed that the tip of V, was up to 5 cm proximal to the frontal projection of the coracoid process. In two subjects we could see that the tips of the V, and V, catheters were positioned in two different veins at the shiulder level (most likely the cephalic and axillary veins). In the other subjects V, was never more than 6 cm proximal to the frontal projection of the coracoid process, and the tips of V, and V, were separated up to 5 cm. The fourth catheter was introduced in a cubital vein of the contralateral arm and advanced proximally to the middle of the upper arm for the determination ofrecirculating dye. Each subject was studied at rest and during 30 min of upright continuous arm bicycle exercise with an increase in intensity every 10 min and at work loads of 30,60, and 90 W. One subject was also studied during 1 h of continuous exercise, for 30 min at 30 W and then for another 30 min at 90 W. Indocyanine green (ICG; Hynson, Westcott, and Dunning, Baltimore, MD) was infused intra-arterially (0.5 mg/ml at an infusion rate of 1 ml/min). The infusions were continued for 5 min in the basal state and for 3 min during exercise. The infusions during exercise started at the 6th min of each work load. For the subject who performed 1 h of continuous exercise, the dye infusions were started at the 6th min of exercise of each work load (30 and 90 W) and were repeated every 4 min. During the dye infusion, six blood samples for ICG analysis were drawn from each of the three vein catheters every 20 s, from 3 min 20 s of infusion to 5 min of infusion at rest and from 1 min 20 s of infusion to 3 min of infusion during exercise.
AND
DURING
ARM
929
EXERCISE
In addition, expired air was collected in Douglas bags for 5 min at rest and during the last 2 min of each work load. 0, saturations and hemoglobin concentrations in arterial and venous blood (V,) were determined at rest and at the end of each work load during exercise. Analyses. ICG (14) was analyzed spectrophotometritally at 805 nm. The readings were made in serum obtained after the clotting and centrifugation of 2.5-ml blood samples. Clot retraction was promoted by incubation of the blood samples for 15 min in a water bath at 37OC. A calibration curve was made for each subject with readings at 4 and 8 mg/l. 0, saturation (6) was determined spectrophotometrically, and hemoglobin was measured by the cyanmethemoglobin method (7). Hematocrit was measured in the same blood specimens that were analyzed for dye concentration by use of a microcapillary hematocrit centrifuge and correction for trapped plasma. Expired air was analyzed mass spectrometrically (9) with a gas analyzer (model MGA 2000, Airspec, Biggin Hill, Kent, UK). The arm blood flow (FJ was calculated from the concentration of the infused dye solution (Ci), the dye concentration in the arm vein (V,) of the infused arm (C,) and of the opposite arm (C,), the rate of infusion (Fi), and hematocrit (Hct), as described earlier for forearm (14) and leg (13) blood flow determinations F
. .- W F,(C * = (c, - C:)(l -“Hct)
With Ci >> C,, the numerator can be approximated to FiCi. FA was calculated as the mean of the six (C, - C,) determinations for each subject at rest and during exerme.
When not otherwise means t SE.
indicated,
values are given as
RESULTS
of method. In the subject in whom fluorocontrol re vealed that the tip of V, was positioned 6
Evaluation SC epic
TABLE
1. Age, height, weight, and vo2 Mean f SE
Range
24.8kO.6 182t2 72.3k2.8 2.13kO.08 3.51t0.14
23-28 177-188 61-84 1.79-2.46 2.89-4.06
61.Ok1.7
55-72
29*1 17+1
25-35 15-20
%i702max(leg)
48k2 28*1
40-56 23-31
max(arm)
78k4
64-89 35-53
Age,Yr
Height, cm Weight, kg 00 2max(arm), l/min (leg), l/min vo2 W’T max I \ "02 mm (arm) %
iToprnax(leg) o. 3”ow
%I702 mm
arm)
(leg)
%vo2 T:xr
max
%V02
max(arm)
cn ou vv
90 w
%VO,
45t2 %vo2 mm(leg) .30 2max9 maximal O2 uptake during arm W 2m8x(leg)] exercise.
[vo2max
(arm)] or leg
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930
ARM BLOOD
FLOW AT REST AND DURING
4
2. Variability of dye concentration between two ipsilateral arm veins after correction for recirculating dye
TABLE
Exercise, Rest
N bean, mgll Range, mgll SD,, mg/l cv, %
60
90
7
5
5
4
764.36 1.9-8.5 1.18 27.1
601.06 0.6-1.7 0.09 8.0
580.53 0.4-1.7 0.02 4.2
480.40 0.4-0.5 0.03 7.1
Values were calculated from mean dye concentrations in V, and VP, on the basis of 5 or 6 samples in each vein from each subject at rest and during exercise. On the basis of differences (D) between these 2 values, variability of dye concentration was calculated as SD, for a single determination, according to the formula SD, = im, where N is no. of subjects, n is no. of blood samples at rest and during exercise, and CV is coefficient of variation calculated as SD, X mean-’ X 100. Mean values and ranges for dye concentrations are representative for all blood samples at rest and during exercise.
cm proximal to the coracoid process, the blood samples of V, showed significantly lower dye concentrations than those of V, at rest but not during exercise. The values for V, in this subject were excluded from the calculations in Table 2. In three subjects V, had to be withdrawn to the middle of the upper arm at some time during exercise because of blood sampling difficulties. Dye concentrations in this position were as much as two times higher than those calculated from V, blood samples and have been excluded in the evaluation of the method. Mixing of dye and blood. Mixing of dye and blood during infusion into the brachial artery was evaluated at rest and during exercise by comparison of the concentration of dye in blood samples obtained from the two ipsilateral arm vein catheters (V, and V,). Corrections were made for recirculation on the basis of the dye concentration in the contralateral vein. The coefficient of variation between V, and V, was as high as 27% at rest but fell to 4-8% during exercise (Table 2). The stability of the dye concentration was evaluated by calculation of the variability in consecutive blood samples from V, after correction for recirculating dye (Table 3). (Analysis of variance showed no difference between these corrected V, values with P of 0.13,0.66, and 0.42 at 30, 60, and 90 W indicating steady-state flows during each measurement.) The coefficient of variation for dye 3. Variability of dye concentration in axillary venous blood after correction for recirculating dye
TABLE
bean, mg/l Range, mgll SD,, mg/l cv, %
l
3ow
l
9ow
W
30
Exercise,
1
ARM EXERCISE
W
Rest
30
60
90
475.09 1.8-10.4 0.42 8.3
480.96 0.5-1.7 0.06 6.3
480.53 0.3-0.8 0.01 2.6
470.41 0.30-0.50 0.01 3.4
Five or 6 samples were drawn from each of 8 subjects for every flow measurement. For each sample, the difference (D) from mean value of 5-6 samples was calculated. See Table 2 footnote for further explanation.
0
10
20
30
Time
40
50
60
(mid
2. Arm blood flow in 1 subject, during 1 h of continuous exercise, 30 min at 30 W and 30 min at 90 W. FIG.
concentration was -8% at rest and 3-6% during exercise (Table 3). The analytic error calculated from multiple analyses of the same blood samples was 0.25% for dye concentrations within the range of 0.7-3.4 mg/l. Duration of infusion. In our experiments, blood sampling was started 3 min 20 s after the onset of dye infusion at rest and 1 min 20 s after that during exercise. The difference in dye concentration between V, and the contralateral vein was adequate for determination of F, in all but one subject, for whom a stable difference was obtained at 1 min 40 s at the lowest work load. Reproducibility. In the one subject who exercised for 1 h (at 30 W for 30 min and then at 90 W for another 30 min), several consecutive measurements of blood flow were made during arm exercise. The results showed consistent blood flow values throughout the exercise period (Fig. 2). Heart rate, arm bloodflow, and O2uptake during continuous exercise of increasing intensity (30, 60, and 90 W).
Heart rate three- and work loads to 29 t 1,
and pulmonary 0, uptake (VO& increased sevenfold, respectively (Tables 4 and 5). The after correction for VO, at rest corresponded 48 t 2, and 78 t 4% of maximal 0, uptake urin arm exercise (Table 1). Mechanical efficiency (ME) for the whole body was 15.9 t 0.2% at the lowest work intensity. ME increased during exercise to 17.9 t 0.7% at the highest work load (P < 0.05). Arm blood flow was measured after 6 min of exercise at each work load. Linear correlations were found between arm blood flow and both work intensity and pulmonary VO, (r = 0.98; Figs. 3 and 4, Table 5). Arm VO, was calculated as the product of arm blood flow and the arteriovenous 0, difference. Arm VO, correlated linearly with work intensity and pulmonary 00, (r = 0.98; Figs. 5 and 6, Table 5). No,,,)
d
l
g
DISCUSSION
No previous reports have been presented on measurements of total arm blood flow during exercise. In the
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ARM BLOOD TABLE
FLOW AT REST AND DURING
ARM EXERCISE
931
4. Circulatory variables for subjects at rest and during exercise of varying intensity During
Exercise
Rest
3ow
60W
9ow
A-WI,, ml/l
56k2 (48-66) 0.24kO.01 (0.19-0.28) 0.85t0.04 (0.72-1.05) 0.21t0.04 (0.11-0.44) 45.6k5.1
Arm 0, uptake, ml/min
(26.8-70.8) 9t2
91t4 (74-105) 0.8OkO.01 (0.73-0.83) 0.98kO.04 (0.84-1.14) 1.09t0.09 (0.64-1.50) 136.6k3.3 (128.3-157.9) 149k12 (88-201)
132+7 (105-160) 1.16kO.04 (0.96-1.29) 0.98t0.03 (0.90-1.20) 1.83t0.10 (1.39-2.18) 131.8k3.8 (116.8-151.9) 241t13 (196-283)
168+_8 (154-200) 1.73kO.07 (1.56-2.11) 1.06t0.03 (0.99-1.17) 2.43t0.14 (1.96-3.16) 133.0t3.3 (125.0-147.7) 323a21 (251-442)
15.9kO.2 (14.9-16.7) 34.Ok3.5 (27.8-56.1)
18.7k0.4 (17.5-20.3) 38.9t2.5 (31.8-47.4)
17.9kO.7 (14.3-19.8) 43.8k2.7 (31.6-56.7)
Heart rate, beats/min Pulmonary O2 uptake, l/min R Arm blood flow, l/min
(5-19)
ME, % Whole body Arm
Values are means k SE for 8 subjects; ranges are in parentheses. R, ventilatory exchange ratio; A-VO,, axillar arteriovenous 0, differences; ME, mechanical efficiency.
present study we propose a constant dye-infusion technique to quantitate total arm blood flow at rest and during exercise. Several conditions must be satisfied. The method requires uniform dispersion of the dye and blood before the sampling site and continuous infusion beyond the longest circulation time in the vascular system studied (16). At this time, constant dye concentration differences will be achieved between the ipsilateral and contralateral arm veins. Complete mixing of blood and dye can occur either on the arterial or the venous side of the vascular system. In this study, the dye was infused into the brachial artery at the level of the midpoint of the upper arm. Some of the arm blood flow might have evaded the dye infused on the arterial side, but the point for blood sample collection on the venous side was chosen to allow prior uniform mixing of the dye with total arm blood flow. To study mixing and equilibration conditions, two ipsilateral venous catheters were inserted in two different cubital arm veins (V, and V,). V, was always the median cubital vein. By external measurements the tips of the catheters were estimated to be separated by ~2-5 cm. Fluoroscopic controls agreed with the external measurements in all but two subjects, in whom it was revealed that the tips of the catheters were positioned in two separate veins at shoulder level. The dye concentrations in these veins were similar, however. The importance of the position of the catheter is illustrated by the results in one subject in whom the V, cathTABLE
eter was positioned 6 cm proximal to the coracoid process. In this subject the dye concentration was approximately one-fourth that in the others at rest, indicating an admixture from thoracic veins. In addition, when in three subjects the V, catheter had to be withdrawn to the middle of the upper arm because of difficulties in blood collection, the dye concentrations became 40% higher than those calculated from the V, samples. The concentrations of dye in the ipsilateral veins proximal to the coracoid process became nearly identical in all subjects during exercise, even for the subject with the tip of the catheter 6 cm proximal to the coracoid process. This indicates that mixing has occurred before the venous sampling site and suggests that the admixture of venous blood from thoracic veins is small during exercise. The increased arm blood flow and probably also the rhythmic muscular movements facilitate mixing of dye and blood. Only one ipsilateral venous catheter seems necessary with a standardized position of the tip within 3-4 cm proximal to the coracoid process, as estimated from external measurements. Fluoroscopic control does not seem necessary for arm flow determinations. For blood sampling, the median cubital vein is to be preferred, inasmuch as no problems were encountered in the collection of blood from this vein. The differences in dye concentrations between the two ipsilateral veins at rest (Table 2), as well as between different V, samples during blood flow determinations (Ta-
5. Relationship of blood flow and arm 0, uptake to work load and pulmonary O2 uptake Work Load, W r
FA, llmin Arm O2 uptake, ml/min
0.980t0.007 (0.947-0.997) 0.975t0.009 (0.928-0.998)
m
0.0246?0.0014* (0.0178-0.0303) 3.45&0.23* (2.46-4.63)
Pulmonary b
0.283t0.045" (0.142-0.494) 25.4k6.4.f (O-51.5)
r
0.982t0.007 (0.948-0.998) 0.979t0.009 (0.941-0.999)
O2 Uptake, m
1.509+0.081* (1.144-1.743) 213.1t11.3' (159.2-246.7)
l/min
STPD b
-0.135+0.070 [0.171-(-0.333)] -33.2+7.3-f. [5.6-(-61)]
Values are means t, SE for 8 subjects; ranges are in parentheses. r, correlation coefficient; m, slope; b, intercept; FA, arm blood flow. Linear regressions are based on formula y = mx + b. Significantly different from zero: * P < 0.001; t P < 0.01. Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (132.174.255.223) on October 10, 2018. Copyright © 1991 American Physiological Society. All rights reserved.
932
ARM 3.5
.E 2 s =
2.5
BLOOD
AT
REST
AND
DURING
-Z .E 2 -
-
I
I
1
1
Rest
30
60
90
Exercise FIG,
FLOW
3. Arm
blood
flow in relation
500
-
400
-
; c, n =I
300-
g cn 5; O E 2
200-
EXERCISE
loo-
Rest
30
to work
intensity
60
Exercise
(W) for 8 subjects.
ble 3), showed that the concentrations of dye could vary considerably. This coefficient of variation is in accord with that previously found for dye concentrations during determinations of resting leg blood flow by a continuous dye-dilution method (13). Because cutaneous blood flow is particularly variable, total arm blood flow as well as the proportions of muscle and skin blood flow in the arm might vary. This is also suggested by the great variability in the arteriovenous 0, difference at rest (Table 4). On the other hand, the high and unchanged arteriovenous 0, difference during exercise (Table 4) indicates only a minor contribution of the cutaneous blood flow, because the 0, saturation in cutaneous veins is >90% (14). Thus the method is more representative of muscle blood flow during exercise. The infusion times and sampling periods in the present study seem to be sufficient to allow equilibration of blood and dye in the whole arm vascular system. Thus 3 min 20 s of infusion at rest before blood sampling appears sufficient for determination of satisfactory resting arm blood flows. During exercise, equilibration was not
5. Arm rest and during FIG.
0, uptake exercise.
in relation
90
(WI
to work
intensity
for 8 subjects
at
reached for one subject until 1 min 40 s of infusion at the lowest work load, and blood sampling during light arm exercise should not start before that time. The arteriovenous 0, difference rose at the lowest work intensity and remained nearly constant at the higher work loads. The increase in arm To2 during exercise was accomplished by an increased blood flow. The same mechanism for increased Vo2 has been described previously for the forearm, where the deep venous blood stemmed almost exclusively from exercising forearm muscle (l4), as well as in other studies comprising leg (2) or both arm and leg (5) exercise. During exercise, VO, in working muscle increases with the requirements. Cardiac output increases and is distributed to supply adequate amounts of blood to the working muscles, and cardiac output and VO, are closely adjusted to the intensity of work. The present findings of linear correlations between arm blood flow or arm yo2 and working intensity (Figs. 3 and 4) or pulmonary VO, (Figs. 5 and 6) are in accord with this. Previous results have demonstrated
3.5 .--c E h
ARM
500
‘2 .E
2
1
400
2.5 -
.
, 0.5
Pulmonary
oxygen
I 1.5
uptake
FIG. 4. Arm blood flow in relation to pulmonary STPD) for 8 subjects at rest and during - exercise.
1
1 2.5
(Vmin) 0, uptake
I
Pulmonary (l/min
I
0.5
I
1
1.5
oxygen
uptake
FIG. 6. Arm 0, uptake in relation to pulmonary STPD) for 8 subjects at rest and during exercise.
2.5
(I/min) O2 uptake
(l/min
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ARM
BLOOD
FLOW
AT
REST
that forearm blood flow and calculated VO, increase linearly in proportion to work intensity (14). The same has been demonstrated for leg blood flow and leg VO, (13). In support of the validity of our measurements, the values for arm blood flow in the present study were 59-49 ml. mine1 W-l compared with 62-52 ml min-’ W-l during leg exercise (13) at work intensities that resulted in similar heart rates. The whole body ME during arm exercise averaged 1619%, in agreement with previous reports for arm exercise (l), a value that is lower than the values during leg exercise, generally reported to be 21-23%. This result suggests that more static (vs. dynamic) work is performed during arm exercise, presumably by trunk muscles, than during leg exercise. On the other hand, the finding of an increasing whole body ME at the two higher intensities suggests that static work does not increase in proportion to the dynamic work. The results could also indicate that more energy is provided by nonoxidative processes during arm exercise. l
l
l
Address for reprint requests: G. Ahlborg, Dept. of Clinical Physiology, Karolinska Hospital, Box 60500, S-10401 Stockholm, Sweden. Received 10 October 1989; accepted in final form 1 October 1990. REFERENCES
1. AHLBORG, G., L. HAGENFELDT, AND J. WAHREN. Substrate utilization by the inactive leg during one-leg or arm exercise. J. Appl. Physiol. 39: 718-723, 1975. 2. ANDERSEN, P., AND B. SALTIN. Maximal perfusion of skeletal muscle in man. J. PhysioZ. Lond. 366: 233-249, 1985. 3. ANDRES, R., K. L. ZIERLER, H. M. ANDERSON, W. N. STAINSBY, G. CADER, A. S. GHRAYYIB, AND J. L. LILIENTHAL. Measurement of blood flow and volume in the forearm of man; with notes on the theory of indicator-dilution and on production of turbulence, hemolysis, and vasodilatation by intra-vascular injection. J. Clin. Invest. 33: 428-504. 1954.
AND
DURING
ARM
933
EXERCISE
H., AND A. C. DORNHURST. Blood flow through the human calf during rhythmic exercise. J. Physiol. Lond. 109: 402411,1949. CLAUSEN, J. P., K. KLAUSEN, B. RASMUSSEN, AND J. TRAP-JENSEN. Central and peripheral circulatory changes after training of the arms or legs. Am. J. Physiol. 225: 675-682,1973. DRABKIN, D. L. Measurement of O,-saturation of blood by direct spectrophotometric determination. Methods Med. Res. 2: 159-162, 1950. DRABKIN, D. L., AND J. H. AUSTIN. Spectrophotometric studies II. Preparations from washed blood cells; nitric oxide hemoglobin and sulfhemoglobin. J. Biol. Chem. 112: 51-65, 1935. GANZ, V., A. HLAVOVA, A. FRONEK, J. LINHART, AND J. PREROVSKY. Measurement of blood flow in the femoral artery in man at rest and during exercise by local thermodilution. Circulation 30:
4. BARCROFT,
5.
6.
7.
8.
86-89,1964. ga.HAFFERL,
ANTON.
Lehrbuch
der Topografischen
Anatomie
(2nd
ed.). Heidelberg: Springer Verlag, 1957. 9. HALLBACK, I., E. KARLSSON, AND B. EKBLOM. Comparison between mass spectrometry and Haldane technique in analysing 0, and CO2 concentrations in air gas mixtures. Stand. J. Clin. Lab. Invest. 38: 285-288, 1978. 10. HLAVOVA, A., J. LINHART, J. PREROVSKY, FRONEK. Leg blood flow at rest, during and after
V. GANZ, AND A. exercise in normal subjects and in patients with femoral artery occlusion. Clin. Sci.
Lond. 29: 555-564,1965. 11. JORFELDT, L. Metabolism of L(+)-lactate in human skeletal muscle during exercise. Acta Physiol. Stand. Suppl. 338: 21-31, 1970. 12. JORFELDT, L., A. JUHLIN-DANNFELT, B. PERNOW, AND E. WAS&N. Determination of human leg blood flow: a thermodilution technique based on femoral venous bolus injection. Clin. Sci. Lond. 54: 517-523,1978. 13. JORFELDT, L., AND J. WAHREN. Leg blood flow during exercise in man. Clin. Sci. Lond. 41: 459-473, 1971. 14. WAHREN, J. Quantitative aspects of blood flow and oxygen uptake in the human forearm during rhythmic exercise. Acta Physiol. Stand. 67, Suppl. 269: l-93, 1966. Human forearm muscle metab15. WAHREN, J., AND L. HAGENFELDT.
olism during exercise. I. Circulatory adaptation to prolonged forearm exercise. Stand. J. Clin. Lab. Invest. 21: 257-262, 1968. K. L. Theory of the use of arteriovenous concentration 16. ZIERLER, differences for measuring metabolism in steady and non-steady states. J. Clin. Invest. 40: 2111-2125, 1961.
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AND
M. JENSEN-URSTAD
of Clinical Physiology, Mdersjukhuset,
AHLBORG, G., AND M. JENSEN-URSTAD. Arm bloodflow at rest and during arm exercise. J. Appl. Physiol. 70(2): 928-933,
1991.-To test the applicability of a dye-dilution method to quantitate total arm blood flow at rest and during arm exercise, indocyanine green was infused at a constant rate into the brachial artery. Eight subjectsperformed continuous 30-min arm exerciseswith an increasein intensity every 10min (30,60, and 90 W). The loads correspondedto 29 t 1,48 k 2, and 78 t 4% (means 2 SE) of the maxima! O2uptake (vozmax 2.13 t 0.08 l/min) during arm exercise. Vozrnarduring arm exercise was 61 -+ 1.7% of that during leg exercise. The dye concentration was analyzed in blood samplesfrom three arm veins, two ipsiand one contralateral, at shoulder level. Corresponding dye concentrations in both ipsilateral veins and a stableconcentration difference between ipsi- and contralateral veins were achieved. Total arm blood flow wascalculated to be 0.21 t 0.04 l/min at rest and 2.43 k 0.14l/min at 90 W. Arm 0, uptake rose from 9 k 2 to 323 & 21 ml/min. Arm blood flow and 0, uptake each correlated linearly with both work load (r = 0.98) and pulmonary 0, uptake (r 2 0.98). Mechanical efficiency for the arm and body was 34-44 and 16-19%, respectively. We conclude that arm blood flow can be determined by continuous infusion of indocyanine green. indocyanine green;pulmonary oxygen uptake; arm oxygen UPtake; mechanicalefficiency
A SUITABLE METHOD for the determination of total arm blood flow is required for the study of arm hemodynamics and application of the Fick principle for quantitations of arm metabolism at rest and during arm exercise with muscles including those of the upper arm. No such method that is applicable both at rest and during exercise has been described before. Several methods are available for forearm or leg blood flow determinations. The venous occlusion meth .od has been used for forearm m.ainly when the a rm is at blood flow determinations rest. It has also been employed for determinations of calf blood flow during rhythmic exercise (4). During exercise,
The thermodilution principle, which has been used for determinations of femoral blood flow at rest as well as during exercise (2,8, 10,12), is probably less suitable for measuring arm blood flow . The method requires that the injection of indicator and temperature measurements be made in the same blood vessel. In this c ontext, the anatomy of the axillary artery and the fact that the axillary vein is not the only vein draining the arm present problems (Fig. 1). 928
0161-7567/91
$1.50
Copyright
S-l 00 64 Stockholm, Sweden
Dye-dilution methods can be designed to circumvent the disadvantages of the thermodilution methods. By application of a dye-dilution technique, the indicator can be infused intra-arterially and measurements can be performed in venous blood, thereby increasing the chances of uniform mixing of the indicator infused with the amount of blood flowing through the arm. Intra-arterial infusion of dye has been used to measure forearm blood flow at rest (3) and during different types of forearm exercises (11, 14, 15). In addition, a constant dye-infusion technique has been employed for measurements of total leg blood flow at rest and during exercise (13). The aim of the present study was to investigate whether it is possible, with the complex vascular system of the arm, to determine total arm blood flow at rest and during arm exercise by a constant infusion of dye into the brachial artery and postmix sampling in the axillary vein. METHODS
Subjects. Eight healthy male subjects were studied in the l2- to 14-h postabsorptive state. The subjects were physically active and well trained but did not participate in competitive athletics. Data on age, body dimensions, and maximal 0, uptake during leg and arm exercise are presented in Table 1. All subjects were informed of the nature, purpose, and possible risks involved in the study before they gave voluntary consent to participate. The procedures in these studies have been reviewed and approved by the institutional Ethics Committee. Procedure. Four thin Teflon catheters (1.0 mm ID, 1.4 mm OD, 600 mm lng) were inserted percutaneously. One catheter was introduced into the right brachial artery in the cubital region and directed 15-20 cm proximally. Another three catheters were inserted at the arm fold in two different arm veins of the ipsilateral arm and in one contralateral arm vein. The position of the ipsilateral venous catheter is of importance because of the possibility of an admixture of blood from vascular beds other than those of the arm. To estimate the influence of the catheter position on the dye concentration, two catheters (V, and V,) were introduced in different veins (V, in the median cubital vein, which is a superficial connection between the cephalic and the basilic vein, and V, in the basilic vein) at the ipsilateral arm fold and positioned up to 5 cm apart with their tips at the level of v. axillaris (Fig. 1). The distance (D) in centimeters from the point of introduction to the coracoid process was estimated so that the catheter could be positioned without fluoroscopic control. The V, tip was inserted at D or up to D + 3 cm. The V, tip was advanced 2-5 cm, but not more than D + 5 cm,
0 1991 the American
Physiological
Society
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ARM
BLOOD
FLOW
AT
REST
v.
FIG. 1. Anatomy of venous system of upper arm. [Adapted from Hafferl (8a) .]
beyond the V, tip. The tips of the ipsilateral catheters were assumed to be somewhere at the level of the confluence of the cephalic and the axillary vein (Fig. 1). To check the catheter positions, fluoroscopic controls were performed and revealed that the tip of V, was up to 5 cm proximal to the frontal projection of the coracoid process. In two subjects we could see that the tips of the V, and V, catheters were positioned in two different veins at the shiulder level (most likely the cephalic and axillary veins). In the other subjects V, was never more than 6 cm proximal to the frontal projection of the coracoid process, and the tips of V, and V, were separated up to 5 cm. The fourth catheter was introduced in a cubital vein of the contralateral arm and advanced proximally to the middle of the upper arm for the determination ofrecirculating dye. Each subject was studied at rest and during 30 min of upright continuous arm bicycle exercise with an increase in intensity every 10 min and at work loads of 30,60, and 90 W. One subject was also studied during 1 h of continuous exercise, for 30 min at 30 W and then for another 30 min at 90 W. Indocyanine green (ICG; Hynson, Westcott, and Dunning, Baltimore, MD) was infused intra-arterially (0.5 mg/ml at an infusion rate of 1 ml/min). The infusions were continued for 5 min in the basal state and for 3 min during exercise. The infusions during exercise started at the 6th min of each work load. For the subject who performed 1 h of continuous exercise, the dye infusions were started at the 6th min of exercise of each work load (30 and 90 W) and were repeated every 4 min. During the dye infusion, six blood samples for ICG analysis were drawn from each of the three vein catheters every 20 s, from 3 min 20 s of infusion to 5 min of infusion at rest and from 1 min 20 s of infusion to 3 min of infusion during exercise.
AND
DURING
ARM
929
EXERCISE
In addition, expired air was collected in Douglas bags for 5 min at rest and during the last 2 min of each work load. 0, saturations and hemoglobin concentrations in arterial and venous blood (V,) were determined at rest and at the end of each work load during exercise. Analyses. ICG (14) was analyzed spectrophotometritally at 805 nm. The readings were made in serum obtained after the clotting and centrifugation of 2.5-ml blood samples. Clot retraction was promoted by incubation of the blood samples for 15 min in a water bath at 37OC. A calibration curve was made for each subject with readings at 4 and 8 mg/l. 0, saturation (6) was determined spectrophotometrically, and hemoglobin was measured by the cyanmethemoglobin method (7). Hematocrit was measured in the same blood specimens that were analyzed for dye concentration by use of a microcapillary hematocrit centrifuge and correction for trapped plasma. Expired air was analyzed mass spectrometrically (9) with a gas analyzer (model MGA 2000, Airspec, Biggin Hill, Kent, UK). The arm blood flow (FJ was calculated from the concentration of the infused dye solution (Ci), the dye concentration in the arm vein (V,) of the infused arm (C,) and of the opposite arm (C,), the rate of infusion (Fi), and hematocrit (Hct), as described earlier for forearm (14) and leg (13) blood flow determinations F
. .- W F,(C * = (c, - C:)(l -“Hct)
With Ci >> C,, the numerator can be approximated to FiCi. FA was calculated as the mean of the six (C, - C,) determinations for each subject at rest and during exerme.
When not otherwise means t SE.
indicated,
values are given as
RESULTS
of method. In the subject in whom fluorocontrol re vealed that the tip of V, was positioned 6
Evaluation SC epic
TABLE
1. Age, height, weight, and vo2 Mean f SE
Range
24.8kO.6 182t2 72.3k2.8 2.13kO.08 3.51t0.14
23-28 177-188 61-84 1.79-2.46 2.89-4.06
61.Ok1.7
55-72
29*1 17+1
25-35 15-20
%i702max(leg)
48k2 28*1
40-56 23-31
max(arm)
78k4
64-89 35-53
Age,Yr
Height, cm Weight, kg 00 2max(arm), l/min (leg), l/min vo2 W’T max I \ "02 mm (arm) %
iToprnax(leg) o. 3”ow
%I702 mm
arm)
(leg)
%vo2 T:xr
max
%V02
max(arm)
cn ou vv
90 w
%VO,
45t2 %vo2 mm(leg) .30 2max9 maximal O2 uptake during arm W 2m8x(leg)] exercise.
[vo2max
(arm)] or leg
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930
ARM BLOOD
FLOW AT REST AND DURING
4
2. Variability of dye concentration between two ipsilateral arm veins after correction for recirculating dye
TABLE
Exercise, Rest
N bean, mgll Range, mgll SD,, mg/l cv, %
60
90
7
5
5
4
764.36 1.9-8.5 1.18 27.1
601.06 0.6-1.7 0.09 8.0
580.53 0.4-1.7 0.02 4.2
480.40 0.4-0.5 0.03 7.1
Values were calculated from mean dye concentrations in V, and VP, on the basis of 5 or 6 samples in each vein from each subject at rest and during exercise. On the basis of differences (D) between these 2 values, variability of dye concentration was calculated as SD, for a single determination, according to the formula SD, = im, where N is no. of subjects, n is no. of blood samples at rest and during exercise, and CV is coefficient of variation calculated as SD, X mean-’ X 100. Mean values and ranges for dye concentrations are representative for all blood samples at rest and during exercise.
cm proximal to the coracoid process, the blood samples of V, showed significantly lower dye concentrations than those of V, at rest but not during exercise. The values for V, in this subject were excluded from the calculations in Table 2. In three subjects V, had to be withdrawn to the middle of the upper arm at some time during exercise because of blood sampling difficulties. Dye concentrations in this position were as much as two times higher than those calculated from V, blood samples and have been excluded in the evaluation of the method. Mixing of dye and blood. Mixing of dye and blood during infusion into the brachial artery was evaluated at rest and during exercise by comparison of the concentration of dye in blood samples obtained from the two ipsilateral arm vein catheters (V, and V,). Corrections were made for recirculation on the basis of the dye concentration in the contralateral vein. The coefficient of variation between V, and V, was as high as 27% at rest but fell to 4-8% during exercise (Table 2). The stability of the dye concentration was evaluated by calculation of the variability in consecutive blood samples from V, after correction for recirculating dye (Table 3). (Analysis of variance showed no difference between these corrected V, values with P of 0.13,0.66, and 0.42 at 30, 60, and 90 W indicating steady-state flows during each measurement.) The coefficient of variation for dye 3. Variability of dye concentration in axillary venous blood after correction for recirculating dye
TABLE
bean, mg/l Range, mgll SD,, mg/l cv, %
l
3ow
l
9ow
W
30
Exercise,
1
ARM EXERCISE
W
Rest
30
60
90
475.09 1.8-10.4 0.42 8.3
480.96 0.5-1.7 0.06 6.3
480.53 0.3-0.8 0.01 2.6
470.41 0.30-0.50 0.01 3.4
Five or 6 samples were drawn from each of 8 subjects for every flow measurement. For each sample, the difference (D) from mean value of 5-6 samples was calculated. See Table 2 footnote for further explanation.
0
10
20
30
Time
40
50
60
(mid
2. Arm blood flow in 1 subject, during 1 h of continuous exercise, 30 min at 30 W and 30 min at 90 W. FIG.
concentration was -8% at rest and 3-6% during exercise (Table 3). The analytic error calculated from multiple analyses of the same blood samples was 0.25% for dye concentrations within the range of 0.7-3.4 mg/l. Duration of infusion. In our experiments, blood sampling was started 3 min 20 s after the onset of dye infusion at rest and 1 min 20 s after that during exercise. The difference in dye concentration between V, and the contralateral vein was adequate for determination of F, in all but one subject, for whom a stable difference was obtained at 1 min 40 s at the lowest work load. Reproducibility. In the one subject who exercised for 1 h (at 30 W for 30 min and then at 90 W for another 30 min), several consecutive measurements of blood flow were made during arm exercise. The results showed consistent blood flow values throughout the exercise period (Fig. 2). Heart rate, arm bloodflow, and O2uptake during continuous exercise of increasing intensity (30, 60, and 90 W).
Heart rate three- and work loads to 29 t 1,
and pulmonary 0, uptake (VO& increased sevenfold, respectively (Tables 4 and 5). The after correction for VO, at rest corresponded 48 t 2, and 78 t 4% of maximal 0, uptake urin arm exercise (Table 1). Mechanical efficiency (ME) for the whole body was 15.9 t 0.2% at the lowest work intensity. ME increased during exercise to 17.9 t 0.7% at the highest work load (P < 0.05). Arm blood flow was measured after 6 min of exercise at each work load. Linear correlations were found between arm blood flow and both work intensity and pulmonary VO, (r = 0.98; Figs. 3 and 4, Table 5). Arm VO, was calculated as the product of arm blood flow and the arteriovenous 0, difference. Arm VO, correlated linearly with work intensity and pulmonary 00, (r = 0.98; Figs. 5 and 6, Table 5). No,,,)
d
l
g
DISCUSSION
No previous reports have been presented on measurements of total arm blood flow during exercise. In the
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ARM BLOOD TABLE
FLOW AT REST AND DURING
ARM EXERCISE
931
4. Circulatory variables for subjects at rest and during exercise of varying intensity During
Exercise
Rest
3ow
60W
9ow
A-WI,, ml/l
56k2 (48-66) 0.24kO.01 (0.19-0.28) 0.85t0.04 (0.72-1.05) 0.21t0.04 (0.11-0.44) 45.6k5.1
Arm 0, uptake, ml/min
(26.8-70.8) 9t2
91t4 (74-105) 0.8OkO.01 (0.73-0.83) 0.98kO.04 (0.84-1.14) 1.09t0.09 (0.64-1.50) 136.6k3.3 (128.3-157.9) 149k12 (88-201)
132+7 (105-160) 1.16kO.04 (0.96-1.29) 0.98t0.03 (0.90-1.20) 1.83t0.10 (1.39-2.18) 131.8k3.8 (116.8-151.9) 241t13 (196-283)
168+_8 (154-200) 1.73kO.07 (1.56-2.11) 1.06t0.03 (0.99-1.17) 2.43t0.14 (1.96-3.16) 133.0t3.3 (125.0-147.7) 323a21 (251-442)
15.9kO.2 (14.9-16.7) 34.Ok3.5 (27.8-56.1)
18.7k0.4 (17.5-20.3) 38.9t2.5 (31.8-47.4)
17.9kO.7 (14.3-19.8) 43.8k2.7 (31.6-56.7)
Heart rate, beats/min Pulmonary O2 uptake, l/min R Arm blood flow, l/min
(5-19)
ME, % Whole body Arm
Values are means k SE for 8 subjects; ranges are in parentheses. R, ventilatory exchange ratio; A-VO,, axillar arteriovenous 0, differences; ME, mechanical efficiency.
present study we propose a constant dye-infusion technique to quantitate total arm blood flow at rest and during exercise. Several conditions must be satisfied. The method requires uniform dispersion of the dye and blood before the sampling site and continuous infusion beyond the longest circulation time in the vascular system studied (16). At this time, constant dye concentration differences will be achieved between the ipsilateral and contralateral arm veins. Complete mixing of blood and dye can occur either on the arterial or the venous side of the vascular system. In this study, the dye was infused into the brachial artery at the level of the midpoint of the upper arm. Some of the arm blood flow might have evaded the dye infused on the arterial side, but the point for blood sample collection on the venous side was chosen to allow prior uniform mixing of the dye with total arm blood flow. To study mixing and equilibration conditions, two ipsilateral venous catheters were inserted in two different cubital arm veins (V, and V,). V, was always the median cubital vein. By external measurements the tips of the catheters were estimated to be separated by ~2-5 cm. Fluoroscopic controls agreed with the external measurements in all but two subjects, in whom it was revealed that the tips of the catheters were positioned in two separate veins at shoulder level. The dye concentrations in these veins were similar, however. The importance of the position of the catheter is illustrated by the results in one subject in whom the V, cathTABLE
eter was positioned 6 cm proximal to the coracoid process. In this subject the dye concentration was approximately one-fourth that in the others at rest, indicating an admixture from thoracic veins. In addition, when in three subjects the V, catheter had to be withdrawn to the middle of the upper arm because of difficulties in blood collection, the dye concentrations became 40% higher than those calculated from the V, samples. The concentrations of dye in the ipsilateral veins proximal to the coracoid process became nearly identical in all subjects during exercise, even for the subject with the tip of the catheter 6 cm proximal to the coracoid process. This indicates that mixing has occurred before the venous sampling site and suggests that the admixture of venous blood from thoracic veins is small during exercise. The increased arm blood flow and probably also the rhythmic muscular movements facilitate mixing of dye and blood. Only one ipsilateral venous catheter seems necessary with a standardized position of the tip within 3-4 cm proximal to the coracoid process, as estimated from external measurements. Fluoroscopic control does not seem necessary for arm flow determinations. For blood sampling, the median cubital vein is to be preferred, inasmuch as no problems were encountered in the collection of blood from this vein. The differences in dye concentrations between the two ipsilateral veins at rest (Table 2), as well as between different V, samples during blood flow determinations (Ta-
5. Relationship of blood flow and arm 0, uptake to work load and pulmonary O2 uptake Work Load, W r
FA, llmin Arm O2 uptake, ml/min
0.980t0.007 (0.947-0.997) 0.975t0.009 (0.928-0.998)
m
0.0246?0.0014* (0.0178-0.0303) 3.45&0.23* (2.46-4.63)
Pulmonary b
0.283t0.045" (0.142-0.494) 25.4k6.4.f (O-51.5)
r
0.982t0.007 (0.948-0.998) 0.979t0.009 (0.941-0.999)
O2 Uptake, m
1.509+0.081* (1.144-1.743) 213.1t11.3' (159.2-246.7)
l/min
STPD b
-0.135+0.070 [0.171-(-0.333)] -33.2+7.3-f. [5.6-(-61)]
Values are means t, SE for 8 subjects; ranges are in parentheses. r, correlation coefficient; m, slope; b, intercept; FA, arm blood flow. Linear regressions are based on formula y = mx + b. Significantly different from zero: * P < 0.001; t P < 0.01. Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (132.174.255.223) on October 10, 2018. Copyright © 1991 American Physiological Society. All rights reserved.
932
ARM 3.5
.E 2 s =
2.5
BLOOD
AT
REST
AND
DURING
-Z .E 2 -
-
I
I
1
1
Rest
30
60
90
Exercise FIG,
FLOW
3. Arm
blood
flow in relation
500
-
400
-
; c, n =I
300-
g cn 5; O E 2
200-
EXERCISE
loo-
Rest
30
to work
intensity
60
Exercise
(W) for 8 subjects.
ble 3), showed that the concentrations of dye could vary considerably. This coefficient of variation is in accord with that previously found for dye concentrations during determinations of resting leg blood flow by a continuous dye-dilution method (13). Because cutaneous blood flow is particularly variable, total arm blood flow as well as the proportions of muscle and skin blood flow in the arm might vary. This is also suggested by the great variability in the arteriovenous 0, difference at rest (Table 4). On the other hand, the high and unchanged arteriovenous 0, difference during exercise (Table 4) indicates only a minor contribution of the cutaneous blood flow, because the 0, saturation in cutaneous veins is >90% (14). Thus the method is more representative of muscle blood flow during exercise. The infusion times and sampling periods in the present study seem to be sufficient to allow equilibration of blood and dye in the whole arm vascular system. Thus 3 min 20 s of infusion at rest before blood sampling appears sufficient for determination of satisfactory resting arm blood flows. During exercise, equilibration was not
5. Arm rest and during FIG.
0, uptake exercise.
in relation
90
(WI
to work
intensity
for 8 subjects
at
reached for one subject until 1 min 40 s of infusion at the lowest work load, and blood sampling during light arm exercise should not start before that time. The arteriovenous 0, difference rose at the lowest work intensity and remained nearly constant at the higher work loads. The increase in arm To2 during exercise was accomplished by an increased blood flow. The same mechanism for increased Vo2 has been described previously for the forearm, where the deep venous blood stemmed almost exclusively from exercising forearm muscle (l4), as well as in other studies comprising leg (2) or both arm and leg (5) exercise. During exercise, VO, in working muscle increases with the requirements. Cardiac output increases and is distributed to supply adequate amounts of blood to the working muscles, and cardiac output and VO, are closely adjusted to the intensity of work. The present findings of linear correlations between arm blood flow or arm yo2 and working intensity (Figs. 3 and 4) or pulmonary VO, (Figs. 5 and 6) are in accord with this. Previous results have demonstrated
3.5 .--c E h
ARM
500
‘2 .E
2
1
400
2.5 -
.
, 0.5
Pulmonary
oxygen
I 1.5
uptake
FIG. 4. Arm blood flow in relation to pulmonary STPD) for 8 subjects at rest and during - exercise.
1
1 2.5
(Vmin) 0, uptake
I
Pulmonary (l/min
I
0.5
I
1
1.5
oxygen
uptake
FIG. 6. Arm 0, uptake in relation to pulmonary STPD) for 8 subjects at rest and during exercise.
2.5
(I/min) O2 uptake
(l/min
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ARM
BLOOD
FLOW
AT
REST
that forearm blood flow and calculated VO, increase linearly in proportion to work intensity (14). The same has been demonstrated for leg blood flow and leg VO, (13). In support of the validity of our measurements, the values for arm blood flow in the present study were 59-49 ml. mine1 W-l compared with 62-52 ml min-’ W-l during leg exercise (13) at work intensities that resulted in similar heart rates. The whole body ME during arm exercise averaged 1619%, in agreement with previous reports for arm exercise (l), a value that is lower than the values during leg exercise, generally reported to be 21-23%. This result suggests that more static (vs. dynamic) work is performed during arm exercise, presumably by trunk muscles, than during leg exercise. On the other hand, the finding of an increasing whole body ME at the two higher intensities suggests that static work does not increase in proportion to the dynamic work. The results could also indicate that more energy is provided by nonoxidative processes during arm exercise. l
l
l
Address for reprint requests: G. Ahlborg, Dept. of Clinical Physiology, Karolinska Hospital, Box 60500, S-10401 Stockholm, Sweden. Received 10 October 1989; accepted in final form 1 October 1990. REFERENCES
1. AHLBORG, G., L. HAGENFELDT, AND J. WAHREN. Substrate utilization by the inactive leg during one-leg or arm exercise. J. Appl. Physiol. 39: 718-723, 1975. 2. ANDERSEN, P., AND B. SALTIN. Maximal perfusion of skeletal muscle in man. J. PhysioZ. Lond. 366: 233-249, 1985. 3. ANDRES, R., K. L. ZIERLER, H. M. ANDERSON, W. N. STAINSBY, G. CADER, A. S. GHRAYYIB, AND J. L. LILIENTHAL. Measurement of blood flow and volume in the forearm of man; with notes on the theory of indicator-dilution and on production of turbulence, hemolysis, and vasodilatation by intra-vascular injection. J. Clin. Invest. 33: 428-504. 1954.
AND
DURING
ARM
933
EXERCISE
H., AND A. C. DORNHURST. Blood flow through the human calf during rhythmic exercise. J. Physiol. Lond. 109: 402411,1949. CLAUSEN, J. P., K. KLAUSEN, B. RASMUSSEN, AND J. TRAP-JENSEN. Central and peripheral circulatory changes after training of the arms or legs. Am. J. Physiol. 225: 675-682,1973. DRABKIN, D. L. Measurement of O,-saturation of blood by direct spectrophotometric determination. Methods Med. Res. 2: 159-162, 1950. DRABKIN, D. L., AND J. H. AUSTIN. Spectrophotometric studies II. Preparations from washed blood cells; nitric oxide hemoglobin and sulfhemoglobin. J. Biol. Chem. 112: 51-65, 1935. GANZ, V., A. HLAVOVA, A. FRONEK, J. LINHART, AND J. PREROVSKY. Measurement of blood flow in the femoral artery in man at rest and during exercise by local thermodilution. Circulation 30:
4. BARCROFT,
5.
6.
7.
8.
86-89,1964. ga.HAFFERL,
ANTON.
Lehrbuch
der Topografischen
Anatomie
(2nd
ed.). Heidelberg: Springer Verlag, 1957. 9. HALLBACK, I., E. KARLSSON, AND B. EKBLOM. Comparison between mass spectrometry and Haldane technique in analysing 0, and CO2 concentrations in air gas mixtures. Stand. J. Clin. Lab. Invest. 38: 285-288, 1978. 10. HLAVOVA, A., J. LINHART, J. PREROVSKY, FRONEK. Leg blood flow at rest, during and after
V. GANZ, AND A. exercise in normal subjects and in patients with femoral artery occlusion. Clin. Sci.
Lond. 29: 555-564,1965. 11. JORFELDT, L. Metabolism of L(+)-lactate in human skeletal muscle during exercise. Acta Physiol. Stand. Suppl. 338: 21-31, 1970. 12. JORFELDT, L., A. JUHLIN-DANNFELT, B. PERNOW, AND E. WAS&N. Determination of human leg blood flow: a thermodilution technique based on femoral venous bolus injection. Clin. Sci. Lond. 54: 517-523,1978. 13. JORFELDT, L., AND J. WAHREN. Leg blood flow during exercise in man. Clin. Sci. Lond. 41: 459-473, 1971. 14. WAHREN, J. Quantitative aspects of blood flow and oxygen uptake in the human forearm during rhythmic exercise. Acta Physiol. Stand. 67, Suppl. 269: l-93, 1966. Human forearm muscle metab15. WAHREN, J., AND L. HAGENFELDT.
olism during exercise. I. Circulatory adaptation to prolonged forearm exercise. Stand. J. Clin. Lab. Invest. 21: 257-262, 1968. K. L. Theory of the use of arteriovenous concentration 16. ZIERLER, differences for measuring metabolism in steady and non-steady states. J. Clin. Invest. 40: 2111-2125, 1961.
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