J Appl Physiol 103: 1950–1957, 2007.
First published October 11, 2007; doi:10.1152/japplphysiol.00452.2007.
Forearm blood flow follows work rate during submaximal dynamic forearm
exercise independent of sex
Joaquin U. Gonzales, Benjamin C. Thompson, John R. Thistlethwaite, Allison J. Harper,
and Barry W. Scheuermann
Cardiopulmonary and Metabolism Research Laboratory, Department of Kinesiology, The University of Toledo, Toledo, Ohio
Submitted 26 April 2007; accepted in final form 5 October 2007
or sustained periods of increased muscle
contractile activity, an increase in muscle perfusion must take
place to deliver oxygen-rich blood to the active mitochondria
as well as to remove metabolic by-products that may lead to
muscle fatigue (11). The close coupling between muscle oxygen consumption and blood flow (3, 17) has been used as
evidence to suggest that local muscle and/or vascular conditions exert considerable feedback regulation over vascular
tone, in addition to the role that sympathetic outflow plays in
maintaining mean arterial pressure (46). The matching of
muscle perfusion to external work rate has been demonstrated
in different muscle groups during isometric and dynamic exercise (1, 16). However, the influence of sex on the blood flow
response to exercise has yet to be fully investigated, although
sex differences in muscle blood flow have been hypothesized
to be a factor contributing to the greater fatigue resistance
observed in women compared with men (21).
To date, the studies that have examined muscle blood flow
during forearm exercise between women and men have relied
primarily on strain-gauge plethysmography (26, 29). For example, it has been reported that women have higher muscle
perfusion and vascular conductance than men following 4 min
of sustained isometric handgrip exercise (26). It has been
postulated that women experience less compressive force and
lower intramuscular pressure on the peripheral vasculature and,
hence, less mechanical hindrance to muscle blood flow compared with men during exercise at the same relative contraction
intensity (21). However, the sex difference in muscle blood
flow is not a consistent finding given that women and men
matched or unmatched for strength show similar muscle blood
flow and vascular conductance when submaximal isometric
handgrip exercise is extended to fatigue (26). In addition, no
sex difference in muscle blood flow was observed following 10
min of dynamic handgrip exercise performed at the same
relative intensity (29). While strain-gauge plethysmography
provides a good estimate of limb blood flow at rest and during
the recovery from exercise, in order for exercise blood flow
responses to be measured, the subject is required to stop
contracting during the exercise (23, 27). Therefore, the extent
that the strain-gauge plethysmography approach reflects muscle blood flow during the actual performance of exercise has
recently been questioned (4). The controversy is further supported by the results of earlier studies that clearly demonstrate
that the occlusion pressure required for obtaining the measurement of blood flow using this technique causes a significant
reduction in muscle blood flow (5, 20).
To circumvent the inherent limitations of other techniques,
the use of Doppler ultrasound has been used to measure
steady-state as well as transient changes in blood flow during
exercise with high temporal resolution (18, 22, 39, 48). However, to our knowledge, the application of Doppler techniques
to investigate possible sex differences in muscle blood flow has
only recently been examined in the leg (36). Therefore, the aim
of the present study was to use Doppler ultrasound to test the
hypothesis that performing dynamic handgrip exercise at the
same work rate (i.e., same absolute intensity but higher relative intensity for women than men) would result in a similar
muscle blood flow response to exercise in women and men,
consistent with a feedback control mechanism balancing metabolic requirements to muscle blood flow. To avoid the confounding influence of tension development on vascular resis-
Address for reprint requests and other correspondence: B. W. Scheuermann,
Dept. of Kinesiology, MS 119, Health and Human Services Bldg., The Univ.
of Toledo, Toledo, OH 43606 (e-mail: [email protected]).
The costs of publication of this article were defrayed in part by the payment
of page charges. The article must therefore be hereby marked “advertisement”
in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
sex differences; forearm blood flow; handgrip; vascular conductance
DURING TRANSIENT
1950
8750-7587/07 $8.00 Copyright © 2007 the American Physiological Society
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Gonzales JU, Thompson BC, Thistlethwaite JR, Harper AJ,
Scheuermann BW. Forearm blood flow follows work rate during
submaximal dynamic forearm exercise independent of sex. J Appl
Physiol 103: 1950–1957, 2007. First published October 11, 2007;
doi:10.1152/japplphysiol.00452.2007.—To test the hypothesis that
sex influences forearm blood flow (FBF) during exercise, 15 women
and 16 men of similar age [women 24.3 ⫾ 4.0 (SD) vs. men 24.9 ⫾
4.5 yr] but different forearm muscle strength (women 290.7 ⫾ 44.4
vs. men 509.6 ⫾ 97.8 N; P ⬍ 0.05) performed dynamic handgrip
exercise as the same absolute workload was increased in a ramp
function (0.25 W/min). Task failure was defined as the inability to
maintain contraction rate. Blood pressure and FBF were measured on
separate arms during exercise by auscultation and Doppler ultrasound,
respectively. Muscle strength was positively correlated with endurance time (r ⫽ 0.72, P ⬍ 0.01) such that women had a shorter time
to task failure than men (450.5 ⫾ 113.0 vs. 831.3 ⫾ 272.9 s; P ⬍
0.05). However, the percentage of maximal handgrip strength
achieved at task failure was similar between sexes (14% maximum
voluntary contraction). FBF was similar between women and men
throughout exercise and at task failure (women 13.6 ⫾ 5.3 vs. men
14.5 ⫾ 4.9 ml 䡠 min⫺1 䡠 100 ml⫺1). Mean arterial pressure was lower in
women at rest and during exercise; thus calculated forearm vascular
conductance (FVC) was higher in women during exercise but similar
between sexes at task failure (women 0.13 ⫾ 0.05 vs. men 0.11 ⫾
0.04 ml 䡠 min⫺1 䡠 100 ml⫺1 䡠 mmHg⫺1). In conclusion, the similar FBF
during exercise was achieved by a higher FVC in the presence of a
lower MAP in women than men. Still, FBF remained coupled to work
rate (and presumably metabolic demand) during exercise irrespective
of sex.
FBF IN WOMEN AND MEN DURING RAMP EXERCISE
tance and impedance to flow as seen during isometric exercise
(2, 42, 45), the subjects performed dynamic muscle contractions with brief periods of mechanical compression followed
by relaxation to allow blood flow to perfuse the muscle
unimpeded during the relaxation phases between contractions
(28, 40).
METHODS
J Appl Physiol • VOL
Blood pressure was measured manually from the left arm by auscultation at the end of every minute for the purpose of monitoring
changes in mean arterial pressure (MAP) with exercise; MAP ⫽
diastolic blood pressure ⫹ 0.33 (systolic blood pressure ⫺ diastolic
blood pressure).
In pilot studies, brachial artery diameter was measured in five
subjects during ramp exercise similar to the protocol used in the
present study. Consistent with the results of others (28, 40, 44), we
found no significant increase in brachial artery diameter during dynamic forearm exercise (see Fig. 2); therefore, resting brachial artery
diameter for each subject was used to calculate blood flow at rest and
during exercise. Brachial artery diameter was measured using a digital
beam-forming ultrasound system (Mysono 201, Medison) operating in
two-dimensional echo mode with a 7.5 MHz/40-mm linear array
probe. Images were recorded on videotape for offline analysis. The
vessel diameter was measured with the arm resting at heart level and
after the subject had rested in the supine position for 15 min. Brachial
artery diameter was determined from longitudinal and cross-sectional
views of the vessel from 10 measurements randomly made where the
vessel walls were most accurately visualized. The mean of these
measurements was then used to calculate an average cross-sectional
area (CSA ⫽ ␲r2) of the artery, where r is the radius of the artery,
which in turn was multiplied by the appropriate blood velocity to
obtain relevant flows (FBF ⫽ blood velocity ⫻ CSA ⫻ 60). In
addition to reporting absolute flow through the brachial artery (FBFa;
ml/min), FBF was also expressed relative to forearm volume (FBFr;
ml 䡠 min⫺1 䡠 100 ml⫺1). For each subject, blood flow was reduced from
beat-to-beat values into 20-s averages for statistical analysis. Forearm
vascular conductance (FVC) was calculated as the ratio of FBFr to
MAP (ml 䡠 min⫺1 䡠 100 ml⫺1 䡠 mmHg⫺1).
Muscle activity was assessed by surface electromyography (sEMG)
obtained from the forearm muscle group using a commercially available data-acquisition system (PowerLab 16SP, ADInstruments). The
analog sEMG signal was sampled at a rate of 2,000 Hz, amplified
(model 408 Dual Bio Amplifier-Stimulator, ADInstruments), passed
through a high-low pass frequency window of 10 –500 Hz, and stored on
a computer for later analysis. The raw sEMG signal was sampled
using bipolar silver-silver chloride electrodes (20-mm-diameter sample area) spaced 40 mm apart on the inside surface of the right forearm
over the digit flexor muscles. A reference electrode was placed over
the bony surface of the ulna near the elbow joint of the left arm.
Electrode sites were shaved and cleaned with alcohol before electrode
placement to reduce interelectrode resistance. All wiring attached to
the electrodes were secured by athletic wrap to prevent movement
artifact, and a notch filter set at 60 Hz was used to minimize noise in
the raw sEMG signal. The sEMG signal was checked for motion
artifact by moving and tapping the area surrounding the electrode. The
site was cleaned again, and a new electrode was applied if any motion
artifact was detected. The raw sEMG signal was analyzed in the time
domain by the root-mean-square method for examination of motor
unit recruitment during exercise. Because of technical difficulties,
sEMG could not be measured in one woman and one man.
Statistical analysis. Anthropometric data along with time to task
failure, end workload, and contraction durations were compared
between women and men by two-sample Student’s t-tests. A two-way
ANOVA with one repeated measure (sex by intensity) was performed
to compare blood velocity, FBF, MAP, FVC, heart rate, relative
contraction intensity, and sEMG within and between women and men
throughout forearm exercise. Because of subjects reaching task failure
at different times (and work loads), comparisons between women and
men were only made at work loads where all subjects contributed to
the group mean (i.e., up to 1.5 W or 3 kg). Statistical significance was
set a priori at P ⱕ 0.05. When a significant main effect or interaction
was observed, a Holm-Sidak post hoc test was used to make multiple
comparisons. The Holm-Sidak methods applies a “step-down” critical
P value approach in determining significance to maximize statistical
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Subjects. Dynamic handgrip exercise was performed in 15 women
(age 24.3 ⫾ 4.0 yr) and 16 men (age 25.9 ⫾ 4.5 yr). Subjects reported
themselves to be either sedentary or recreationally active, and all
subjects reported not having any metabolic, cardiovascular, and pulmonary disease as assessed through a standard medical history questionnaire. The study was approved by the Human Subjects Research
Committee at The University of Toledo and is in accordance with
guidelines set forth by the Declaration of Helsinki of The World
Medical Association. All subjects provided written informed consent
after being explained all experimental procedures, the exercise protocol, and possible risks associated with participation in the study. All
testing was performed in the Cardiopulmonary and Metabolism Research Laboratory at The University of Toledo.
Experimental protocol. Subjects were asked to refrain from strenuous physical activity for 24 h before each study session, especially
physical activities involving the use of the forearm muscles. On a
separate day before any exercise testing, anthropometric measurements including forearm volume and maximal forearm muscle
strength were measured by water displacement and using a handgrip
dynamometer (Takei), respectively. The average of three maximal
voluntary isometric contractions (MVC) was used as the value of
forearm muscle strength. No less than 2 min of recovery was allowed
between each MVC effort to avoid any effects of fatigue.
On the day of exercise testing, subjects rested in the supine position
with both forearms at heart level for at least 15 min before resting
forearm blood flow (FBF) was measured in the right brachial artery.
Handgrip exercise was performed in the supine position with the right
forearm extended to a custom-built arm ergometer. The arm ergometer allowed for 10 cm of distance traveled during each concentric
contraction phase, which was recorded by a potentiometer incorporated into the pulley system (see Fig. 1A). This allowed for the offline
analysis of contraction duty cycle, frequency, and durations (contraction and relaxation time). The exercise protocol consisted of 2 min of
unloaded forearm muscle contractions followed by a ramp increase in
work load (0.5 kg/min) as applied by the constant flow of water into
a bucket at the end of the pulley system that was calibrated before
exercise testing. Task failure was defined as the inability of subjects
to maintain contraction frequency and/or duty cycle during handgrip
exercise. Contraction frequency was set at 30 contractions/min, which
subjects followed with an audio metronome, and dynamic contraction
duty cycle was set for a short contraction cycle duration that was
easily learned and adhered to by the subjects.
Measurements. Instantaneous blood velocity (cm/s) in the right
brachial artery was continuously measured using a Doppler ultrasound
velocimetry system (model 500-M, Multigon Industries) operating in
pulsed mode. The pulsed-wave Doppler transducer, with an operating
frequency of 4 MHz and fixed transducer crystal and sound beam
angle of 45° relative to the skin, was placed flat on the inside of the
right arm 6 –10 cm above the inner humeral condyle, above and
parallel to the brachial artery. Blood velocity was measured in all
subjects by one researcher exhibiting a between-day and test-retest
coefficient of variation of 10.4% and 6.4%, respectively. Electrocardiography (ECG) was obtained using a modified three-lead placement.
Brachial artery blood velocity was averaged over each cardiac cycle
between R-R wave intervals using software described in a previous
study (22). The continuous cardiovascular (blood velocity, ECG)
and ergometer data (displacement) were digitized (ADInstruments,
PowerLab 16SP, Grand Junction, CO) and stored for offline analysis.
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FBF IN WOMEN AND MEN DURING RAMP EXERCISE
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Fig. 1. Raw data collected from a representative subject while
performing dynamic handgrip contractions. A: distance traveled
during each muscle contraction was measured so that contraction
duration, duty cycle, and contraction frequency could be calculated. Surface electromyography (sEMG) of the forearm muscles
(B) and brachial artery blood velocity (C) were continuously
measured during exercise. Note that the mechanical compression
associated with each forearm muscle contraction changed the
blood velocity pattern from forward (antegrade) flow to reverse
(retrograde) flow. D: forearm blood flow (FBF) was calculated
from the product of blood velocity and artery cross-sectional area
measured at rest. Note the effect of absolute force on the FBF
oscillations as the subject progresses from unloaded contractions
(UC) to exercise with larger workloads.
power without increasing the risk of making a type I error (14). Values
are expressed as means ⫾ SD unless stated otherwise.
RESULTS
Subjects. Subject anthropometric characteristics are presented and compared between women and men in Table 1.
There was no sex difference in age, but women were on
average shorter, weighed less, had a lower body mass index
(BMI), lower forearm muscle mass, and smaller brachial artery
diameter than men. Forearm muscle volume and strength was
35% and 43% lower in women than men, respectively. Muscle
strength was linearly related to forearm volume (r ⫽ 0.89, P ⬍
J Appl Physiol • VOL
0.01, pooled data) such that subjects with larger forearms
produced greater handgrip strength. Brachial artery diameter
was also related to forearm volume (r ⫽ 0.61, P ⬍ 0.01, pooled
data).
Ramp test performance. The duration of contraction (women
0.27 ⫾ 0.05 vs. men 0.24 ⫾ 0.03 s, P ⫽ 0.07) and the duration
of relaxation between contractions (women 1.74 ⫾ 0.05 vs.
men 1.76 ⫾ 0.03 s, P ⬎ 0.05) were similar between women
and men. On average, women had a shorter time to task failure
than men (women 450.5 ⫾ 113.0 vs. men 831.3 ⫾ 272.9 s, P ⬍
0.05) that resulted in a lower (P ⬍ 0.05) peak work load at task
failure for women (2.1 ⫾ 0.4 W; 4.2 ⫾ 0.8 kg) than men
103 • DECEMBER 2007 •
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FBF IN WOMEN AND MEN DURING RAMP EXERCISE
1953
(3.6 ⫾ 0.9 W; 7.4 ⫾ 1.9 kg). Despite this difference, women
and men reached task failure at a similar percentage of maximal muscle strength (women 14.3 ⫾ 2.5 vs. men 14.2 ⫾
2.1%MVC, P ⬎ 0.05). The time to task failure was correlated
to both forearm muscle strength (r ⫽ 0.84, P ⬍ 0.01, pooled
data) and forearm volume (r ⫽ 0.69, P ⬍ 0.05, pooled data).
Hemodynamic response to dynamic handgrip exercise. The
effect of dynamic forearm muscle contractions on blood velocity is shown for a representative subject in Fig. 1, along with
the FBF response to a ramp increase in work load (Fig. 1D).
Mean blood velocity was not different between women and
men at rest and throughout the ramp increase in work load
except at task failure where men had faster blood velocities
than women (Fig. 3A). Similarly, resting FBFa tended to be
lower (P ⫽ 0.06) in women (17.4 ⫾ 12.4 ml/min) than men
(28.2 ⫾ 17.7 ml/min) but was not different between the sexes
throughout handgrip exercise (Fig. 3B). At task failure, FBFa
was lower in women compared with men (women 109.8 ⫾
39.7 vs. men 185.8 ⫾ 69.0 ml/min, P ⬍ 0.05) because of the
higher work load achieved by men at end exercise. A significant positive correlation was observed between FBFa and work
load at end exercise (r ⫽ 0.48, P ⬍ 0.05, pooled data).
When FBF was expressed relative to forearm volume, no sex
difference was present in FBFr at rest (women 2.0 ⫾ 1.2 vs.
men 2.1 ⫾ 0.9 ml䡠min⫺1 䡠100 ml⫺1, P ⬎ 0.05), throughout
handgrip exercise, or at task failure (women 13.6 ⫾ 5.3 vs.
Table 1. Anthropometric data for women and men
Ag, yr
Height, cm
Weight, kg
BMI, kg/m2
Forearm muscle mass, kg
Forearm muscle volume, ml
Isometric MVC, N
Brachial artery diameter, cm
Women (n ⫽ 15)
Men (n ⫽ 16)
24.3⫾4.0
163.9⫾6.3*
61.5⫾9.2*
22.8⫾2.5*
0.26⫾0.05*
836.9⫾185.7*
290.7⫾44.4*
0.37⫾0.05*
24.9⫾4.5
178.0⫾7.3
79.5⫾11.5
25.0⫾2.6
0.40⫾0.09
1,291.9⫾282.6
509.6⫾97.8
0.42⫾0.04
Values are means ⫾ SD. BMI, body mass index; MVC, maximum voluntary
traction. *Value significantly lower in women than men (P ⬍ 0.05).
J Appl Physiol • VOL
Fig. 3. Comparison of mean blood velocity (A), absolute FBF (FBFabs), and
relative muscle perfusion (FBFrel) between women and men across handgrip
workloads during the ramp test. Men showed a greater blood velocity and
FBFabs than women at task failure (TF) because of the larger workload
achieved (3.6 vs. 2.1 W, respectively). *Significant difference between women
and men (P ⬍ 0.05).
men 14.5 ⫾ 4.9 ml䡠min⫺1 䡠100 ml⫺1, P ⬎ 0.05) (Fig. 3C). No
sex difference was found in resting heart rate or the heart rate
response to dynamic handgrip exercise. In contrast, MAP was
lower (P ⬍ 0.05) in women than men at rest and throughout
handgrip exercise although the percent increase in MAP from
rest was not different between sexes during handgrip exercise
except for task failure where men showed a greater percent
increase in MAP than women (Table 2). To normalize FBFr to
the sex difference in MAP, FVC was calculated and found to
be similar between women and men at rest (women 0.02 ⫾
0.01 vs. men 0.02 ⫾ 0.01 ml䡠min⫺1 䡠100 ml⫺1 䡠mmHg⫺1, P ⬎
0.05) but was higher in women than men during handgrip
exercise (Table 2). No sex difference was found in FVC at task
failure (women 0.13 ⫾ 0.05 vs. men 0.11 ⫾ 0.04
ml䡠min⫺1 䡠100 ml⫺1 䡠mmHg⫺1, P ⬎ 0.05).
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Fig. 2. Brachial artery diameter measured in a subgroup of subjects (n ⫽ 5, 1
woman, 4 men) during the ramp increase in handgrip workload. ANOVA
testing did not find a significant change in brachial artery diameter during
exercise (P ⫽ 0.81).
1954
FBF IN WOMEN AND MEN DURING RAMP EXERCISE
Table 2. Relative contraction intensity, forearm muscle activity, heart rate, blood pressure response, and forearm vascular
conductance changes during a ramp increase in handgrip work load for women and men
Rest
0.50 W
0.75 W
1.0 W
1.25 W
1.50 W
1.7⫾0.2
1.0⫾0.2
3.4⫾0.5
2.0⫾0.5*
5.2⫾0.7
3.0⫾0.7*
6.9⫾0.9
4.0⫾0.9*
8.6⫾1.2
5.0⫾1.2*
10.3⫾1.4
6.0⫾1.4*
14.3⫾2.5
14.2⫾2.1
155⫾45
160⫾50
184⫾57
197⫾87
198⫾68
222⫾93
247⫾90
250⫾116
315⫾134
289⫾149
351⫾136
319⫾158
425⫾149
528⫾302
64⫾5
61⫾12
68⫾9
68⫾13
75⫾10
70⫾13
76⫾9
71⫾11
76⫾9
72⫾11
80⫾10
72⫾11
82⫾8
74⫾11
87⫾9
93⫾14
83⫾6
96⫾11†
87⫾9
99⫾10†
89⫾9
101⫾12†
90⫾9
103⫾9†
92⫾8
104⫾10†
93⫾9
106⫾10†
96⫾8
108⫾10†
104⫾8
124⫾12†
4.4⫾4.8
3.4⫾3.2
6.6⫾4.8
5.3⫾5.5
8.1⫾4.2
8.2⫾5.1
9.9⫾4.6
9.0⫾3.2
11.6⫾5.6
10.8⫾4.5
14.9⫾5.9
12.8⫾5.9
24.7⫾8.0
30.4⫾11.6†
0.06⫾0.03
0.04⫾0.02
0.08⫾0.03
0.05⫾0.02
0.10⫾0.04
0.06⫾0.02*
0.11⫾0.05
0.07⫾0.02*
0.12⫾0.05
0.08⫾0.03*
0.12⫾0.05
0.09⫾0.03*
0.13⫾0.05
0.11⫾0.04
0.02⫾0.01
0.02⫾0.01
Task Failure
Values are means ⫾ SD. UC, unloaded contraction; MAP, mean arterial pressure; FVC, forearm vascular conductance. *Value significantly higher in women
than men (P ⬍ 0.05). †Value significantly lower in women than men (P ⬍ 0.05).
Forearm muscle activity. The increase in sEMG was significantly correlated with exercise work load (r ⫽ 0.52, P ⬍ 0.05,
pooled data); hence, no sex difference was found in forearm
muscle activity during dynamic handgrip exercise (Table 2). At
task failure, women and men demonstrated a similar increase
in sEMG when expressed as a percent change from unloaded
contractions (women 425.6 ⫾ 149.1 vs. men 528.8 ⫾ 302.9%,
P ⬎ 0.05).
DISCUSSION
The aim of the present study was to test the hypothesis that
sex differences influence muscle blood flow during exercise.
To this end, Doppler ultrasound was used to measure FBF in
women and men during progressive dynamic handgrip exercise
to fatigue where the slope of the ramp function was the same
for both sexes (i.e., same absolute task but lower relative task
for men than women). In agreement with our original hypothesis, the significant findings of the present study suggest that
muscle blood flow remains well-matched to work rate and
presumably the metabolic demand of the exercising muscle
in a manner independent of sex. First, FBF during submaximal exercise, expressed either as conduit flow (FBFa, ml/
min) or muscle perfusion relative to forearm volume (FBFr,
ml䡠min⫺1 䡠100 ml⫺1), was not different between women and
men, despite considerable differences in forearm muscle size
and strength. Second, in contrast to the similar FBF responses,
FVC was greater in women than men during submaximal
exercise, which can be attributed primarily to the lower MAP
in women compared with men. Finally, since FBFa matched
work rate during submaximal exercise, FBFa was higher in
men than women at task failure because of the greater absolute
work load achieved by men at task failure. Additionally, FBFr
appears to be coupled to the relative contractile demands of
muscle as indicated by the similar muscle perfusion measured
in women and men at task failure when both sexes ended
exercise at the same relative contraction intensity (i.e., ⬃14%
of their respective MVCs). The speculation that sex differences
in relative contraction intensity, and hence vascular occlusion
J Appl Physiol • VOL
to muscle blood flow during exercise, are partly responsible for
sex differences in exercise tolerance is not supported by the
results of the present study.
Forearm blood flow is similar between women and men. The
regulation of skeletal muscle blood flow during exercise is
controlled by central and peripheral factors, including the
metabolic requirements of the active muscle. Since metabolic
demands are proportional to exercise work rate, it is reasonable
to assume that the similar slope of the ramp function used in
the present study for women and men yielded a similar increase
in work rate as resistance was progressively added. The results
of the present study demonstrated a close coupling between
FBFa and the increase in metabolic demand of the forearm
muscles and that this association was similar for women and
men. These findings are in agreement with previous studies
demonstrating a close matching between oxygen consumption
and muscle blood flow during exercise (1, 3, 16, 17), and
suggests that metabolic requirements may outweigh any potential hemodynamic advantage women may have due to sex
differences in contraction-induced changes in intramuscular
pressure or local vasomotor control factors such as nitric oxide
bioavailability (12).
Forearm blood flow, when expressed as conduit flow (FBFa,
ml/min), exhibits a close coupling to absolute work load as
demonstrated by two findings. First, a significant correlation
was present between FBFa and exercise work load such that
FBFa increased in a linear fashion with the progressive increase in handgrip work load. Second, FBFa was higher in men
than women at task failure, which is consistent with the higher
work load achieved by the men compared with the women. On
the other hand, blood flow expressed relative to forearm
volume (FBFr, ml䡠min⫺1 䡠100 ml⫺1), was not correlated with
absolute work load but was associated with the relative contraction intensity. Evidence for this relationship can be found
in the similar FBFr between women and men at task failure
where both sexes ended exercise at 14% MVC. The similar
relative increase in forearm muscle activity at task failure
suggests that FBFr follows muscle mass recruitment during
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Relative intensity, %MVC
Women
Men
sEMG, %UC
Women
Men
Heart rate, beats/min
Women
Men
MAP, mmHg
Women
Men
MAP, %change from rest
Women
Men
FVC, ml 䡠 min⫺1 䡠 100 ml⫺1 䡠 mmHg⫺1
Women
Men
0.25 W
FBF IN WOMEN AND MEN DURING RAMP EXERCISE
J Appl Physiol • VOL
higher resting systolic and diastolic blood pressure than women
(group average systolic/diastolic blood pressure: men 128/82
vs. women 108/72), although both sexes were normotensive.
On the basis of the equation we used to calculate MAP, we
believe the higher resting MAP in men than women in the
present study was due to the significant sex difference in
diastolic blood pressure.
Despite the sex difference in absolute MAP, the percent
increase in MAP from rest was not different between women
and men during handgrip exercise. Only at task failure when
men exercised longer and achieved a higher exercise work load
was the percent increase in MAP higher in men than women.
This suggests that brachial artery control during dynamic
handgrip exercise involved sympathetic outflow to the artery
that adjusted MAP in proportion to exercise intensity in an
identical fashion between women and men. Considering that
the contractile demand and forearm muscle activity was the
same between women and men in the present study, it is
reasonable to speculate that comparable levels of muscle metabolites were produced by women and men during exercise,
which would lead to reflex sympathetic activation (8). In
contrast to autonomic vasoconstrictor signals, the higher FVC
in women compared with men suggests that vasodilatory signals within the forearm microcirculation (local vasodilation)
may have been greater or the vasculature more sensitive to
these signals in women than men during exercise. This may be
a sex difference found in other limbs considering that women
have also been shown to have a greater vascular conductance
in the femoral artery during incremental knee extension exercise (36). Evidence for sex differences in vascular reactivity is
provided by studies that report a greater flow-mediated vasodilation and vasoconstriction in women than men (6, 31).
Animal research also reports sex differences in the sensitivity
of the vasculature to endothelial-dependent agonists that vary
between arteries (30). Nevertheless, the higher FVC allowed
women to achieve the same FBF response as men during
exercise. This information adds to the literature by demonstrating sex differences in the control of muscle blood flow during
dynamic handgrip exercise, which recent studies suggest may
vary with age (38).
Sex differences in exercise tolerance. Time to task failure
was ⬃85% longer in men than women during dynamic handgrip exercise performed in a ramp function (0.5 kg/min). Our
findings are in agreement with previous literature reporting
muscle strength to be positively related to absolute endurance
time during dynamic exercise. Using bench press exercise,
Shaver (43) found muscle strength to be significantly related
(r ⫽ 0.93) to the number of repetitions subjects could perform
with a common work load set at 75% of the group’s mean
MVC force. However, when work load was set relative to each
subjects maximal strength (i.e., 75% of each individual’s
MVC), muscle strength was no longer significantly correlated
to the number of repetitions completed (r ⫽ ⫺0.19). In the
same manner, the present study found forearm muscle strength
to be significantly correlated with time to task failure (r ⫽
0.84) for exercise performed with a common increase in
absolute work load. However, if exercise tolerance were to be
defined as the percentage of maximal force capacity achieved
at task failure, then muscle strength would no longer be
associated with exercise tolerance since the contractile force
measured at task failure corresponded to ⬃14% MVC for both
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exercise irrespective of absolute work load. Together, these
findings indicate that FBFa increases in proportion to the
intensity of muscular activity, and presumably metabolic rate,
while FBFr increases with muscle mass recruitment during
exercise.
Our findings of a similar FBFa response between women
and men during handgrip exercise is in partial agreement with
the results of a recent study that examined sex differences in
femoral artery blood flow during incremental single-leg knee
extension exercise. Parker et al. (36) found femoral blood flow
to be similar between sexes at low work loads (⬍15 W) but
was higher for women than men at moderate to high work
loads (15– 40 W). The authors attributed the sex difference in
femoral blood flow in part to a proportionately larger increase
in femoral artery diameter during exercise in women than men.
Also, it was reasoned that a lower hemoglobin concentration in
women than men may have contributed to the higher exercise
hyperemia consequent to the lower arterial oxygen content of
the blood. In contrast to these findings, the results of our pilot
studies indicate that brachial artery diameter remains relatively
unchanged from resting values, at least at the relatively low
work loads (⬍5 W) achieved by our subjects. It is possible that
sex differences in FBF may be elicited if higher work loads
could be achieved during dynamic handgrip exercise before
fatigue.
In the present study, the increase in sEMG was not significantly different between women and men during dynamic
exercise. In contrast to dynamic exercise, Hunter et al. (24) has
shown men to have a higher rate of increase in sEMG than
women during static isometric exercise, although the total
increase in sEMG at task failure was similar between sexes.
This sex difference in the pattern of muscle activity indicates
that muscle mass recruitment is different between women and
men during isometric exercise. Since the increase in sEMG
during isometric exercise is associated with increased intramuscular pressure (9), it follows that sex differences in motor
unit recruitment would result in different levels of muscle
perfusion during exercise since intramuscular pressure is
known to reduce muscle perfusion during exercise (42). In this
manner, we believe the lower muscle perfusion in men than
women reported by Hunter et al. (26) is the result of sex
differences in the muscle mass recruited at the time of blood
flow measurement (4 min into an isometric handgrip contraction). This is in agreement with a recent study by Thompson
et al. (47) that reported similar FBF and sEMG responses
between women and men during static isometric handgrip
exercise at a low contraction intensity. The similar rise in
forearm muscle activity along with FBFr between women and
men in the present study supports this relationship.
Vascular conductance is greater in women than men. A
significant sex difference was found in FVC such that women
had a higher FVC than men during dynamic handgrip exercise.
This difference was in the presence of a lower MAP in women
than men. Sex differences in MAP are not a consistent finding
although men are frequently reported to have a higher resting
blood pressure, particularly systolic blood pressure, than
women (32, 33). This sex-related difference in blood pressure
may be due to sex differences in body mass (34), a lower tonic
sympathoadrenal activity in women than men (7), or the effect
of sex hormones (estrogen and progesterone) on blood pressure
regulation (41). In the present study, men had significantly
1955
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FBF IN WOMEN AND MEN DURING RAMP EXERCISE
J Appl Physiol • VOL
contractile force deficit was not assessed. Nonetheless, FBFa
increased with an increase in work load up to task failure and
was not different between women and men. The absence of a
plateau or decrease in FBF during handgrip exercise suggests
that FBF was not a factor limiting exercise tolerance. This is in
agreement with a recent report that found the onset of muscle
fatigue, as assessed by periodic measurements of MVC force,
to occur before the plateau in blood flow occurred during
intermittent isometric dorsiflexor exercise (50).
Last, menstrual cycle phase was not controlled for in the
women tested in this study. Although menstrual cycle phase
(i.e., estrogen levels) has a significant influence on vascular
reactivity (19), recent studies suggest that menstrual cycle
phase may not significantly influence the response of muscle
blood flow to exercise in humans. For instance, Hunter et al.
(26) recently reported no association between the day of the
menstrual cycle in women and measures of forearm blood flow
and vascular conductance taken at rest and postcontraction
from isometric handgrip exercise. Furthermore, Lynn et al.
(32) did not find the increase in femoral blood flow following
cycling exercise at 60% of peak O2 consumption to be different
between menstrual cycle phases or between women and men.
On the basis of these results, we do not believe that menstrual
cycle phase played a significant influence on our study results.
Still, vascular reactivity to a flow-mediated stimulus has been
shown to be dependent on menstrual cycle phase and differ
between sexes (19); therefore we cannot discount the possibility that menstrual cycle phase had an influence on the study
findings.
Conclusions. The experimental approach used in the present
study required women and men to exercise at the same absolute
work rate and, presumably, metabolic demand. Our results find
that FBF, whether expressed as conduit artery flow or normalized to forearm volume, was not different between women and
men during dynamic handgrip exercise. The similar FBF response to exercise was achieved by a higher FVC in the
presence of a lower MAP in women than men. Last, the sex
difference in time to task failure despite the similar FBF
response to exercise suggests that muscle blood flow does not
determine exercise tolerance during this dynamic handgrip
exercise.
GRANTS
J. U. Gonzales was supported by National Heart, Lung, and Blood Institute
Grant 5-F31-HL-077996.
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