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J Appl Physiol 101: 140-150, 2006. First published April 6, 2006; doi:10.1152/japplphysiol.01567.2005
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Active hyperemia and vascular conductance differ between men and women for an isometric fatiguing contraction

Sandra K. Hunter, Jennie M. Schletty, Kristine M. Schlachter, Erin E. Griffith, Aaron J. Polichnowski, and Alexander V. Ng

Exercise Science Program, Department of Physical Therapy, Marquette University, Milwaukee, Wisconsin

Submitted 13 December 2005 ; accepted in final form 16 March 2006


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
To understand the role of muscle perfusion in the sex differences of muscle fatigue, we compared the time to task failure, postcontraction (active) hyperemia, and vascular conductance for an isometric fatiguing contraction performed by young men and women with the handgrip muscles at 20% of maximal voluntary contraction (MVC) force. In study 1, the men (n = 16) were stronger than the women (n = 18), and study 2, the men (n = 7) and women (n = 7) were matched for strength. Isometric contractions were sustained during two sessions: 1) until the target force could no longer be achieved or 2) for 4 min. For both studies, blood flow and vascular conductance were similar for the men and women at rest and after 10 min of occlusion, and at task failure for the fatiguing contraction estimated using forearm venous occlusion plethysmography. In study 1, the time to task failure was longer for the women (11.4 ± 2.8 min) than for the men (8.4 ± 2.4 min; P = 0.003). However, at the end of the 4-min contraction, active hyperemia and vascular conductance were greater for the men than the women (99 vs. 70% peak blood flow; P < 0.001). In study 2, the men and women had similar strength and a similar time to failure (8.4 ± 1.6 vs. 8.6 ± 2.3 min). Active hyperemia was greater for the men than the women (86 vs. 64% peak flow; P = 0.038) after the 4-min contraction, as was vascular conductance (80 vs. 57% peak conductance; P = 0.02). Thus the briefer time to failure of men than women for an isometric fatiguing contraction is a function of the greater strength of men but is not dependent on differences in the active hyperemia and vascular conductance.

muscle fatigue; gender; skeletal muscle blood flow; handgrip; venous occlusion plethysmography

YOUNG WOMEN ARE ABLE TO MAINTAIN an isometric contraction for a longer duration than men when performed at the same relative intensity (8, 9, 21, 23, 45, 47, 55) (for review see Ref. 17). The sex difference in muscle fatigue may involve a reduced blood flow and oxygen supply to the muscle for the men, who are usually stronger than women due to larger intramuscular pressures and mechanical compression of the blood vessels (2, 46, 48). Accordingly, the sex difference in muscle fatigue was not exhibited when blood flow was occluded to the muscle for maximal contractions of the plantar flexor muscles (45) and a sustained submaximal contraction of the quadricep muscles (8). These studies suggest that that the sex difference in muscle fatigue is exhibited only when the muscle perfusion is apparent.

For submaximal contractions that are sustained with the elbow flexor muscles, the target force exerted during the contraction and the time to task failure are inversely related (21, 23), and the pressor response is greater for the stronger men compared with women, who are usually weaker (23). Consequently, the time to task failure, pressor response, and muscle fatigue were similar when men and women were matched for strength (16, 22). The pressor response is an increase in mean arterial pressure (MAP) due to central command and the peripheral metaboreflex (1, 34, 44) and will increase rapidly during sustained contractions in an attempt to rectify the mismatch of blood flow that becomes progressively occluded during sustained contractions (43). Consistent with these findings, blood flow is more occluded at higher intensity contractions in the same individual (2, 20, 48, 56) and also in stronger men than weaker men when the relative intensity is similar (2). However, blood flow has not been compared in men and women during sustained isometric contractions when performed at the same relative intensity.

To understand the hemodynamics of isometric contractions in men and women, we quantified postcontraction (active) hyperemia using venous occlusion plethysmography (27, 56) along with blood pressure measurements and calculated vascular conductance in men and women. This technique is a well-established and reliable method for determining increased blood flow (hyperemia) immediately after isometric contractions (27), which is inversely associated with the muscle perfusion during the contraction (20, 42, 56). Therefore, those individuals who have greater hyperemia and vascular conductance immediately after a sustained isometric contraction likely have less perfusion during the contraction.

The purpose of this study was to compare the time to task failure, active hyperemia, and vascular conductance for a sustained isometric contraction performed at a submaximal intensity by young men and women with the handgrip muscles when the men were stronger than the women and also in a group of men and women who were matched for strength. We quantified active hyperemia and calculated vascular conductance in men and women after 1) a series of brief nonfatiguing submaximal isometric contractions at various intensities, and 2) at task failure and at the same absolute time (4 min) for a sustained contraction maintained at 20% of maximal strength for both young men and women. We hypothesized that when the men were stronger than the women (study 1), the men would have greater active hyperemia and vascular conductance than the women, who exerted less absolute force when measured at the same absolute time after a submaximal fatiguing contraction of similar relative intensity and that this would be associated with the time to task failure. Pilot data indicated that a 4-min contraction was able to be sustained by most subjects before failure of the task and was a long enough duration that fatigue developed in both men and women. An absolute time point was chosen to compare the blood flow because this represents different stages of fatigue for the men and women due to the progressive occlusion that occurs during a submaximal contraction as the force is maintained and more motor units are recruited. For the men and women who were matched for strength (study 2), we hypothesized that the time to failure, active hyperemia, and vascular conductance would be similar immediately after the 4-min contraction and the sustained contraction held until failure. Strategies used by the men and women to perform the tasks were characterized by additional measurements, including electromyographic (EMG) activity of finger flexor muscles, MAP, heart rate, and rating of perceived exertion (RPE) during the fatiguing isometric contractions. Preliminary results were presented in abstract form (26).


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Sixteen young men (21.9 ± 2.2 yr) and 18 young women (21.6 ± 1.7 yr) volunteered to participate in study 1 when the men were stronger than the women. Seven young men (22.9 ± 6.8 yr) and seven young women (21.0 ± 2.6 yr) who were matched for strength volunteered for study 2. Three men and three women who participated in study 1 were also matched for strength and included in study 2. All subjects were healthy with no known neurological or cardiovascular diseases and were naive to the protocol. Before participation in the study, each subject provided informed consent and the Institutional Review Board at the Marquette University approved the protocol. All subjects who participated in studies 1 and 2 performed the same procedures and experimental protocol.

The physical activity level for each subject was assessed with a questionnaire (30) that estimated the relative kilocalorie expenditure of energy per week. Arm dominance was estimated using the Edinburgh Handedness Inventory (39); all subjects were right handed. The day of the menstrual cycle on which the experimental protocol was performed was recorded for each female participant. This was recorded to determine whether the strength, time to task failure, or active hyperemia was related to the menstrual cycle. The first day of menstruation was considered as day 1 of the cycle.

Mechanical Recording

Subjects were seated upright in an adjustable chair with the nondominant arm abducted at the shoulder and the elbow resting on a padded support. The elbow joint was flexed to 90° so that the forearm was horizontal to the ground, and the hand was placed slightly above heart level with the wrist resting on a padded support and with the hand gripping a handgrip dynamometer (Lafayette Instrument, Lafayette, IN). The adjustable handgrip dynamometer recorded the forces exerted by the finger flexors and was mounted to a rigid restraint so that the subject's hand and forearm were midway between pronation and supination. The forces detected by the transducer were recorded online using Biopac MP30 Pro (Bipoac System, Goleta, CA) and displayed on monitor located 1.6 m in front of the subject. The force signal was digitized at 1,000 samples/s.

Electrical Recordings

EMG was recorded to ensure each subject performed no forearm contraction during measurement of blood flow and to give a global measure of muscle activation of the finger flexor muscles during the sustained contractions. The EMG signal was recorded with bipolar surface electrodes (Ag-AgCl, 8-mm diameter; 16 mm between electrodes) that were placed over the belly of the finger flexor muscles (anterior forearm) about one-third the distance of the forearm proximal to the antecubital fossa, which in turn was proximal to the plethysmography strain gauge. A reference electrode was placed on a bony prominence at the elbow. Care was taken to standardize electrode locations between subjects and sessions. The EMG signal was amplified (1,000x) and band-pass filtered (13–1,000 Hz) with a bioamplifier (Coulbourn Instruments, Allentown, PA) before being recorded directly to computer using the Power 1401 A-D converter [Cambridge Electronic Design (CED), Cambridge, UK]. The EMG signal was digitized at 2,000 samples/s.

Cardiovascular Measurements

Heart rate and blood pressure were monitored during measurement of resting and peak forearm blood flow, throughout the fatiguing contraction, and during active hyperemia after contractions with an automated, beat-by-beat blood pressure monitor (Finapres 2300, Ohmeda, Madison, WI). The blood pressure cuff was placed around the middle finger of the relaxed, dominant hand with the arm placed on a table adjacent to the subject at heart level. Manual blood pressure was taken at the brachial artery to confirm the readings with the Finapres when the hand was placed at heart level. The blood pressure signal was recorded online to computer at 500 samples/s.

Forearm Blood Flow

The subject was seated in the same position as for the mechanical recordings for all blood flow measurements. Each subject was seated upright in an adjustable chair with the nondominant arm abducted at the shoulder and the elbow resting on a padded support so that the arm was at or above heart level. The elbow joint was flexed to 90° so that the forearm was horizontal to the ground, and the hand was placed slightly above heart level with the wrist resting on a padded support.

Resting measurements.   Forearm blood flow was measured noninvasively using venous occlusion plethysmography (27, 40). A double-stranded mercury-in-Silastic strain gauge was positioned around the largest circumference of the forearm and connected to an electrically calibrated and self-balancing plethysmograph (EC-6 Plethysmograph, D. E. Hokanson). Data from the plethysmograph were sampled at 200 Hz (Power 1401, CED) and recorded directly to computer. A venous occlusion cuff was positioned proximal to the elbow and connected to a rapid and adjustable cuff inflator air source (E-20 Rapid Cuff Inflator and AG-101 Air Source, D. E. Hokanson). A wrist cuff was manually inflated to 300 mmHg 1 min before all blood flow measurements to prevent blood flow to the hand. Resting forearm blood flow was measured repeatedly over 3 min by inflating the venous occlusion cuff to 50 mmHg for 8 s and deflating for 7 s. Thus 12 resting blood flow measurements were obtained. Blood pressure was monitored continuously, and the venous occlusion cuff pressure was maintained lower than diastolic blood pressure (DBP). A cuff pressure of 50 mmHg was chosen because it resulted in the most linear slope (40).

Passive arterial occlusion.   Passive arterial occlusion of the forearm was used to determine peak blood flow and vascular conductance (40). Occlusion was administered by inflating the occlusion cuff to suprasystolic pressures (200 mmHg) for 10 min. At 9 min of occlusion, the wrist cuff was inflated to 300 mmHg. At 10 min, the occlusion cuff was deflated and then rapidly inflated to 50 mmHg. Forearm blood flow was then measured every 15 s for 3 min with the first measurement being obtained within 10 s of cuff deflation.

Experimental Protocol

Each subject visited the laboratory for an introductory session to become familiar with the equipment and performance of maximal voluntary contractions (MVC) and then returned for two additional sessions. The protocol for the experimental sessions comprised: 1) measurement of resting blood flow; 2) measurement of peak blood flow after 10 min of occlusion with an inflatable cuff at the upper arm; 3) an assessment of the MVC force for the handgrip muscles after full recovery from the occlusion; 4) performance of submaximal isometric tasks for determination of the hyperemic response and EMG-force relations for 6-s contractions sustained at 20, 40, 60, and 80% of MVC force; 5) performance of a fatiguing contraction sustained at 20% of MVC maintained until task failure (task failure contraction) or for 4 min (4-min contraction) each followed by measurement of the hyperemic response; and 6) an MVC performed with the handgrip muscles within 20 s of completing the fatiguing contraction.

MVC force.   Each subject performed three MVC trials with the handgrip muscles. The MVC task consisted of an increase in force from zero to maximum over 1–2 s, with the maximal force held for 2–3 s. The force exerted by the hand was displayed on a monitor, and each subject was verbally encouraged to achieve maximal force. There was a 60-s rest between trials. If the peak forces from two of the three trials were not within 5% of each other, additional trials were performed until this was accomplished. The greatest force achieved by the subject was taken as the MVC force and used as the reference to calculate the target level for the brief submaximal contractions at 20, 40, 60, and 80% MVC force and the 20% MVC sustained contraction.

Brief submaximal contractions.   Each subject performed a sustained constant-force contraction with the handgrip muscles for 6 s at target values of 20, 40, 60, and 80% of MVC force. At 5 s, a cuff that was placed at the wrist of the arm performing the contraction was inflated to 300 mmHg to occlude blood flow to the hand (40). The subject was then asked to relax, and the upper arm cuff was inflated to 50 mmHg to determine the active hyperemic response to the brief contraction. The cuff was inflated within 2 s after completion of the contraction. The contractions were performed in a randomized order, and the subject was given a 60-s rest between each contraction. These submaximal contractions were performed to 1) determine the active hyperemia and vascular conductance in the men and women in the nonfatigued state across each experimental day at various relative intensities of contraction, and 2) record the EMG activity of the finger flexor muscles so that the EMG-force relation could be compared across days and between the men and women in the nonfatigued state. These relations for the men and women were examined to ensure that changes in EMG, active hyperemia, and vascular conductance during the fatiguing contraction and at task failure represented physiological adjustments and were not due to differences in recording conditions across the experimental days. The EMG signal was also examined to ensure the subject was relaxed during the measurement of blood flow.

Fatiguing contractions.   On one of the experimental days, a fatiguing contraction of the elbow flexor muscles was performed at a target value of 20% MVC force and was sustained until failure (task-failure contraction). The subject was required to match the target force as displayed on the monitor and was verbally encouraged to sustain the force for as long as possible. The fatiguing contraction was terminated when the force declined by 10% of the target value for greater than ~3 s. Neither the subject nor the investigator who terminated the contraction knew the time during the task. At the other experimental session, the subject maintained the 20% MVC target force for 4 min (4-min contraction). Active hyperemia was measured at cessation of both sustained contractions by inflating the wrist cuff to 300 mmHg to occlude blood flow to the hand, asking the subject to completely relax and inflating the upper arm cuff to 50 mmHg for 8 s. The cuff was inflated within 2 s after termination of the fatiguing contraction. An absolute time of 4 min was chosen to measure active hyperemia and vascular conductance to test our hypothesis that women who are weaker than men and have a longer time to failure for a submaximal isometric contraction would be more perfused than men when measured at the same absolute time. Pilot data indicated that the stronger men were able to sustain the contraction for at least 4 min when performed at 20% of MVC force before failure of the task.

During the fatiguing contractions, an index of perceived effort, the RPE, was assessed with the modified Borg 10-point scale (3). The subjects were instructed to focus the assessment of effort with the forearm muscles performing the task. The scale was anchored so that 0 represented the resting state and 10 corresponded to the strongest contraction that the forearm muscles could perform. The RPE was measured at 30-s intervals during the fatiguing contraction.

Data Analysis

The blood flow data, mean arterial pressure, and EMG activity collected during the experiments were analyzed offline using the Spike2 data-analysis system (CED), and the force was analyzed offline using Biopac MP30 Pro (Bipoac System).

The MVC force was quantified as the peak value achieved during the MVC. Similarly, the maximal EMG was determined as the average value over a 0.5-s interval that was centered about the peak rectified EMG. The rectified EMG of the constant-force contractions performed at 20, 40, 60, and 80% of MVC force was averaged over the first 3 s of the 6-s contraction. The EMG activity during the task-failure contraction and 4-min contraction was quantified as averages of the rectified EMG (AEMG) over the first 15 s of the task; 7.5 s on both sides of 25, 50, and 75% of the task; and the last 15 s of the task. The EMG was normalized to the peak EMG obtained during the MVC.

Heart rate and MAP recorded during the task failure contraction and 4-min contraction were analyzed by comparing ~15 s averages at 25% intervals throughout the fatiguing contraction. For each interval, the blood pressure signal was analyzed for the mean peaks [systolic blood pressure (SBP)], mean troughs (DBP), and the number of pulses per second (multiplied by 60 to determine heart rate). MAP was calculated for each epoch with the following equation: MAP = DBP + (SBP – DBP).

Blood flow analysis.   Blood flow analysis was performed as previously reported (40). Blood flow was analyzed (Spike 2, CED) from the slope of the initial, linear portion of the plethysmographic signal. For resting measurements, this included the entire portion of the signal, whereas for forearm blood flow after passive arterial occlusion, the 6-s submaximal contractions, and the sustained fatiguing contractions, the initial two to four heartbeats contained the linear portion of the signal. All blood flow data were analyzed by placing two cursors around the linear portion of plethysmographic signal, and the corresponding slope was calculated using a data-analysis software program. Forearm blood flow (ml·min–1·100 ml–1) was derived using the following equation:

Formula
Vascular conductance (ml·min–1·100 ml–1·mmHg–1) was calculated as blood flow/MAP. For resting measurements, this included averaging the 12 blood flow measurements obtained divided by the average MAP during the 3-min collection period. Forearm vascular conductance after contraction was calculated by dividing each blood flow measurement by the average of MAP that occurred over a 10-s time period that started and ended 1 s either side of the 8 s cuff inflation. Peak vascular conductance was the highest calculated value of the blood flow/10-s average of MAP after cuff deflation. Peak conductance occurred within the first 45 s or the first blood flow measurements after release of the cuff after 10 min of occlusion. The highest blood flow and vascular conductance measured after 10 min occlusion were used as peak blood flow and peak vascular conductance, respectively.

Statistical Analysis

Data are reported as means ± SD within the text and table, and they are displayed as means ± SE in the figures. Separate ANOVAs (SPSS version 13.0) were used to compare the time to task failure and percent decline in MVC force after the fatiguing contraction for the men and women. Repeated-measures ANOVAs were used to compare the dependent variables of forearm blood flow and vascular conductance at the termination of the task failure and 4-min contractions, heart rate, MAP, RPE, force-EMG relation, and force-blood flow relation for the 6-s constant-torque contractions. Post hoc analyses (independent t-tests) were used to test for differences when appropriate. Associations were determined between some variables using Pearson's correlation analysis. Because of the expected multiple bivariate correlations of dependent to independent variables and among dependent variables, stepwise linear regression was used to gain insight into the predictive nature and contribution of dependent variables to the total variation of the time to task failure (SPSS version. 13). Reliability analysis was conducted on some resting measures, and the intraclass correlations (ICC) was reported. For all analyses, a significance level of P < 0.05 was used to identify statistical significance.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
In study 1, the men were stronger than the women and in study 2 the men and women were matched for strength.

Study 1: Men Stronger than Women

The young men were taller than the young women (184 ± 9 vs. 164 ± 6 cm; P < 0.001) and had greater body mass than the women (86.2 ± 12 vs. 66.8 ± 10 kg; P < 0.001). The reported level of physical activity was variable but similar for men [76 ± 58 metabolic equivalents (MET)·h/wk] and women (54 ± 60 MET·h/wk; P = 0.30).

MVC force.   Maximal handgrip force for the young men was greater than the young women when performed before the 4-min sustained contraction (495 ± 67 vs. 300 ± 47 N, respectively; P < 0.001) and the task failure contraction (500 ± 64 vs. 306 ± 57 N, respectively; P < 0.001). Thus the young men exerted greater absolute force than the women when the brief contractions were performed at 20, 40, 60, and 80% of MVC force and during the sustained contractions at 20% of MVC force. There was no difference in MVC force between the 2 experimental days for the men or women (P = 0.79). The day-to-day reliability (ICC) for the MVC was 0.99. The reductions in MVC strength performed after the task failure contraction were significant (P < 0.001) but similar for the men and women (33 ± 9 vs. 36 ± 11%, respectively; P = 0.64).

Time to task failure.   The time to task failure was longer for the women (11.4 ± 2.8 min) compared with the men (8.4 ± 2.4 min; P = 0.003). There was an inverse relation between absolute force exerted during the contractions and the time to failure for the fatiguing contraction (r = 0.62, r2 = 0.39, P < 0.001) such that those individuals who were stronger had a briefer time to failure for the fatiguing contraction (Fig. 1). When the men and women were analyzed separately, the relation remained for the women (r = –0.52, P = 0.01) but not for the men (r = –0.32, P = 0.11).


Figure 1
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  		Fig. 1. Relation between the target force exerted during the fatiguing contraction and time to failure of the men (n = 16) and women (n = 18) for study 1. Time to failure increased linearly as the target force exerted by the finger flexors muscles declined (r = 0.62, P < 0.001). The equation for the relation is y = 16.4 – 0.082x [i.e., time to failure (min) = 16.4 – 0.082 x target force (N)].

 
Stepwise linear regression analysis was performed to determine the predictors of time to task failure. The only significant predictors of time to task failure were MVC force before the task and the EMG activity at task failure. MVC force explained 39% of the variance in time to failure (r = 0.62, P < 0.001), and together the MVC force and EMG activity accounted for 46% of the variance (r = 0.68, P < 0.05). Other dependent variables that were entered into the model but were not significant included active hyperemia and vascular conductance at task failure and for the 4-min contraction, height, weight, physical activity levels, RPE, MAP, and heart rate.

Blood flow and vascular conductance.   RESTING.   The measures of resting MAP, forearm blood flow, and vascular conductance were similar across the experimental days (P > 0.05) and were similar for the men and women (P > 0.05). Data are presented in Table 1. Furthermore, there was no interaction of experimental day and sex (P > 0.05) for any of the variables measured. The day-to-day reliability (ICC) for resting MAP was 0.81, for forearm blood flow was 0.47, and for vascular conductance was 0.48, indicating a modest degree of day-to-day variability within a subject for the blood flow measurements.


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  		Table 1. Resting MAP, forearm blood flow, and vascular conductance for the men and women at the different experimental sessions

 
PEAK.   Peak blood flow and vascular conductance was determined in response to 10 min of passive occlusion on both experimental days. Peak flow was similar across experimental days (P = 0.34) and for the men and women (P = 0.36) with no interaction of sex and day (P = 0.82). The peak blood flow for the women was 38.1 ± 10.5 ml·min–1·100 ml–1 on the day the 4-min contraction was performed and 39.3 ± 7.9 ml·min–1·100 ml–1 on the day of the task-failure contraction. For men, peak blood flow was 40.2 ± 9.5 ml·min–1·100 ml–1 on the 4-min contraction day and 42.2 ± 9.0 ml·min–1·100 ml–1 on the day of the task-failure contraction.

Peak vascular conductance of the forearm was similar for the men and women (P = 0.60) across both days (0.505 ± 0.13 ml·min–1·100 ml–1·mmHg–1; P = 0.58). There was no interaction of sex and experimental day (P = 0.82). The peak vascular conductance for the women was 0.486 ± 0.15 ml·min–1·100 ml–1·mmHg–1 on the 4-min contraction day and 0.504 ± 0.12 ml·min–1·100 ml–1·mmHg–1 on the day of the task-failure contraction. Similarly, the men had a peak conductance of 0.511 ± 0.12 ml·min–1·100 ml–1·mmHg–1 on the 4-min contraction day and 0.519 ± 0.12 ml·min–1·100 ml–1·mmHg–1 on the day of the task-failure contraction.

Blood flow and vascular conductance after 6-s submaximal contractions.   Active hyperemia and vascular conductance were assessed on each experimental day in response to 6-s contractions performed at 20, 40, 60, and 80% of MVC force. There was a main effect of sex because the women had less blood flow compared with the men after the brief isometric contractions at each relative force level and on both days (Fig. 2A; P = 0.04). There was no interaction between the experimental day, sex, or force level (P = 0.58). However, blood flow was progressively greater with the increase in force for both the men and women after each contraction (P < 0.001).


Figure 2
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  		Fig. 2. Blood flow (A) and vascular conductance (B) after submaximal contractions maintained at 20, 40, 60, and 80% of maximal voluntary contraction (MVC) force for 6 s by men who were stronger than the women. The data for each experimental day (4-min contraction day and task failure contraction day) is pooled because there was no difference across the experimental days (P > 0.05). The men had greater active hyperemia and vascular conductance after each contraction compared with the women (P < 0.05).

 
Similarly, the women had less vascular conductance after the submaximal contractions compared with the men for each experimental day and for each contraction force (main effect of sex, P = 0.02; Fig. 2B). There were no differences in vascular conductance after the submaximal contractions performed on the day of the 4-min contraction (0.330 ± 0.11 ml·min–1·100 ml–1·mmHg–1) compared with task-failure contraction (0.330 ± 0.13 ml·min–1·100 ml–1·mmHg–1; P = 0.52). Furthermore, there was no interaction for sex, day, and force level (P = 0.66). However, similar to that for the blood flow, forearm vascular conductance was progressively greater with the increase in force for both the men and women (P < 0.001). The men had greater vascular conductance after the 20% (0.264 ± 0.10 ml·min–1·100 ml–1·mmHg–1), 40% (0.341 ± 0.07 ml·min–1·100 ml–1·mmHg–1), 60% (0.402 ± 0.08 ml·min–1·100 ml–1·mmHg–1), and 80% (0.446 ± 0.11 ml·min–1·100 ml–1·mmHg–1) MVC force levels compared with the women for the contractions at 20% (0.216 ± 0.08 ml·min–1·100 ml–1·mmHg–1), 40% (0.283 ± 0.09 ml·min–1·100 ml–1·mmHg–1), 60% (0.350 ± 0.11 ml·min–1·100 ml–1·mmHg–1), and 80% (0.373 ± 0.11 ml·min–1·100 ml–1·mmHg–1) MVC force.

TASK-FAILURE CONTRACTION.   Men and women had similar blood flow and vascular conductance at task failure. The blood flow after the task-failure contraction for the women was 39.6 ± 10.4 ml·min–1·100 ml–1 (100 ± 18% of peak flow) and for the men was 45.3 ± 10.9 ml·min–1·100 ml–1 (103 ± 18% of peak flow; P = 0.68; Fig. 3A). Similarly, forearm conductance was similar for the men (0.426 ± 0.10 ml·min–1·100 ml–1·mmHg–1, 79 ± 13% of peak conductance) and women (0.383 ± 0.10 ml·min–1·100 ml–1·mmHg–1, 76 ± 17% of peak conductance) at task failure (P = 0.52, Fig. 3B).


Figure 3
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  		Fig. 3. Blood flow and (A) and vascular conductance (B) measured immediately after the 20% fatiguing contraction for men and women (study 1). At task failure, both men and women had similar active hyperemia (P > 0.05). However, at 4 min (48 and 35% of time to failure for men and women, respectively), the women had significantly lower active hyperemia and vascular conductance compared with men and compared with blood flow at task failure (*P < 0.05).

 
4-MIN CONTRACTION   Because the women had a longer time to failure than the men, the 4-min contraction was 35% of the time to failure for the women and 48% for the men (P = 0.004). The blood flow after the 4-min contraction for the women (26.8 ± 7.7 ml·min–1·100 ml–1, 70 ± 17% of peak flow) was significantly lower compared with the blood flow for the men (39.7 ± 10.4 ml·min–1·100 ml–1, 99 ± 21% of peak flow; P < 0.001; Fig. 3A). Furthermore, the blood flow for the women after the 4-min contraction was less than their values at task failure (indicated by an interaction of sex and task, P = 0.005) but not so for the men.

Similarly, forearm vascular conductance was greater for the men (0.427 ± 0.16 ml·min–1·100 ml–1·mmHg–1, 83 ± 20% of peak conductance) compared with the women (0.288 ± 0.09 ml·min–1·100 ml–1·mmHg–1, 59 ± 17% of peak conductance) at the completion of the 4-min contraction (P = 0.002; Fig. 3B). Women also had lower conductance at the end of the 4-min contraction compared with that at task failure (P = 0.01) but not so for the men.

Target force exerted during the 4-min contraction was associated with blood flow (r = 0.59, P < 0.001) and vascular conductance (r = 0.46, P = 0.003) such that the stronger men and women had greater active hyperemia and conductance at termination of the 4-min contraction (Fig. 4A). Furthermore, the time to failure was negatively associated with the blood flow (r = –0.37, P = 0.015; Fig. 4B) and vascular conductance (r = –0.34, P = 0.026) after the 4-min contraction such that those men and women who had a longer time to task failure had less active hyperemia and vascular conductance. However, the significance of the relation appears driven by one data point (male subject on right side of Fig. 4B). When this data point was excluded from the analysis, time to task failure and blood flow were not associated (r = 0.24, P = 0.09).


Figure 4
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  		Fig. 4. Relations between the absolute blood flow after a 4-min contraction with target force exerted during the 20% contraction (A) and time to failure for the same intensity contraction (B) for study 1.

 
There was no association between the day of the menstrual cycle for the women and any of the blood flow or vascular conductance measures taken at rest, after 10 min of occlusion, and postcontraction (P > 0.05). Furthermore, there was no association of the day of menstrual cycle with the time to task failure or with the strength of the woman (P > 0.05).

MAP and heart rate during the fatiguing contractions.   MAP increased for both men and women during the fatiguing contractions on each experimental day (P < 0.001; Fig. 5). The men and women had similar MAP values at the start and end of the task-failure contraction (P = 0.87). Similarly, for the 4-min contraction, the men and women had similar MAP values at the start and end of the contraction (P = 0.21).


Figure 5
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  		Fig. 5. Mean arterial pressure (MAP) during the fatiguing contraction for the men and women (study 1). Values are means ± SE of 15-s intervals at 25% increments of the time failure for the men and women (circles) and every minute during the 4-min contraction (triangles). The men and women started and ended the fatiguing contraction at similar values of MAP (P > 0.05).

 
Heart rate also increased during the 4-min contraction and task-failure contraction for both men and women (P < 0.001). However, the increase in heart rate was similar for the men and women for the task-failure contraction (P = 0.53) and 4-min contraction (P = 0.86). The men and women had similar heart rate values at the start (75 ± 9 and 79 ± 13 beats/min, respectively) and end (98 ± 16 and 99 ± 19 beats/min, respectively) of the task-failure contraction. For the 4-min contraction, the men and women had a similar heart rate at the start (71 ± 9 and 74 ± 11 beats/min, respectively) and end of the contraction (80 ± 10 and 77 ± 11 beats/min, respectively), with no interaction of sex and time (P = 0.12)

RPE.   RPE increased during the fatiguing contraction (P < 0.001), but it was similar for men and women at the beginning and end of the fatiguing contraction held to task failure (P = 0.96). The RPE values for the men and women progressed from 1.3 ± 0.9 and 1.1 ± 0.6, respectively, at the start of the contraction to 9.9 ± 0.4 and 10 ± 0.1 at task failure. However, the rate of increase in the RPE was more gradual for the women due to the longer duration of the contraction. During the 4-min contraction, the RPE increased for the men and women (P < 0.001). At the start of the 4-min contraction, RPE for men and women was 1.1 ± 0.6 and 0.9 ± 0.5, respectively, and at 4 min was 6.0 ± 1.8 and 5.2 ± 2.1, respectively (P = 0.16).

EMG activity   EMG-FORCE RELATION.   The AEMG (%peak EMG) for the finger flexor muscles was determined during 6-s isometric contractions held at 20, 40, 60, and 80% of MVC force on the 2 experimental days. AEMG increased with contraction intensity on both days (P < 0.05) similarly for the men and women (P > 0.05). There were also no differences in the AEMG across days. For the men and women pooled, the AEMG for the 20, 40, 60, and 80% of MVC was 10 ± 4, 21 ± 8, 33 ± 10, and 53 ± 14%, respectively, on the day the task-failure contraction was performed and 10 ± 3, 22 ± 5, 37 ± 10, and 55 ± 8% on the day of the 4-min contraction.

AEMG DURING THE FATIGUING CONTRACTION.   The amplitude of the AEMG (%peak EMG) for finger flexor muscles increased during both fatiguing contractions for the men and women (P < 0.05). The AEMG was similar at the start and end of the fatiguing contraction held until failure for both sexes: the AEMG was 9 ± 4% for the men and 11 ± 4% for the women at the start and was 26 ± 7% for the men and 23 ± 10% for the women at the end of the fatiguing contraction. Similarly, the AEMG for the men and women were similar at the start (9 ± 2 and 10 ± 2%, respectively) and end (13 ± 4 and 13 ± 5%, respectively) of the 4-min contraction.

Study 2: Strength-Matched Men and Women

In study 2, the time to task failure, active hyperemia and vascular conductance were compared in men and women matched for handgrip strength. The men and women were of similar age (22.9 ± 6.8 vs. 21.0 ± 2.6 yr; P = 0.51), height (168 ± 4 vs. 168 ± 12 cm; P = 0.96), body mass (71.0 ± 17 vs. 72.2 ± 23 kg; P = 0.80), and physical activity level (94 ± 79 vs. 66 ± 59 MET·h/wk; P = 0.50). Pairs of men and women were matched for strength so that each man and woman who was matched exerted an MVC force that was within 5% of each other (3 pairs were retrospectively matched from study 1). Consequently, the maximal handgrip force for the strength-matched men and women was similar (367 ± 47 vs. 359 ± 45 N; P = 0.83) before the 4-min task and fatiguing task sustained until failure (359 ± 51 vs. 367 ± 41 N, respectively; P = 0.66). The time to task failure was similar for the men (8.4 ± 1.6 min) and strength-matched women (8.6 ± 2.3 min; P = 0.85).

Blood flow and vascular conductance.   RESTING.   The measures of resting MAP, forearm blood flow, and vascular conductance were similar across the experimental days (P > 0.05) and were similar for the strength-matched men and women (P > 0.05; Table 1).

PEAK.   There was no difference in peak blood flow between the strength-matched men and women (P = 0.97) or across experimental days (P = 0.57). The peak blood flow for the women was 41.9 ± 7.7 ml·min–1·100 ml–1 on the day the 4-min contraction was performed and 37.7 ± 7.8 ml·min–1·100 ml–1 on the day of the task-failure contraction. For men, peak blood flow was 39.8 ± 13.4 ml·min–1·100 ml–1 on the 4-min contraction day and 41.0 ± 8.1 ml·min–1·100 ml–1 on the day of the task-failure contraction.

Peak vascular conductance of the forearm was similar for the strength-matched men and women (P = 0.54) across both days (P = 0.52) with no interaction of sex and experimental day (P = 0.21). The peak vascular conductance for the women was 0.500 ± 0.12 ml·min–1·100 ml–1·mmHg–1 on the 4-min contraction day and 0.448 ± 0.13 ml·min–1·100 ml–1·mmHg–1 on the day of the task failure contraction. Similarly, the men had a peak conductance of 0.469 ± 0.16 ml·min–1·100 ml–1·mmHg–1 on the 4-min contraction day and 0.495 ± 0.15 ml·min–1·100 ml–1·mmHg–1 on the day of the task-failure contraction.

6-S SUBMAXIMAL CONTRACTIONS.   There was an increase in active hyperemia (blood flow and percentage of peak blood flow; P < 0.001) with contraction force, but this was similar across days for both men and women (P = 0.63). The men had similar blood flow compared with the strength-matched women after the brief isometric contractions at each force level on both days (P = 0.24). Similarly, vascular conductance increased with contraction force (P < 0.001) and was similar for men and women on both days of testing (P = 0.71). Vascular conductance was similar for the strength-matched men and women (P = 0.53; Fig. 6A).


Figure 6
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  		Fig. 6. Blood flow (B) and vascular conductance (A and C) measured immediately after contraction in the strength-matched men and women (study 2). Values are means ± SE. A: vascular conductance was similar for strength-matched men and women after submaximal contractions maintained for 6 s. B and C: at task failure, both men and women had similar active hyperemia (P > 0.05). However, at 4 min (48 and 47% of time to failure for men and women, respectively), the women had significantly lower active hyperemia (B) and vascular conductance (C) compared with the strength-matched men (*P < 0.05).

 
FATIGUING CONTRACTIONS.   At task failure blood flow was similar for the men (39.6 ± 11.9 ml·min–1·100 ml–1, 95 ± 13% of peak blood flow) and strength-matched women (35.3 ± 12.1 ml·min–1·100 ml–1, 93 ± 27% of peak blood flow; P = 0.84; Fig. 6B). Forearm conductance was also similar for the men (0.365 ± 0.13 ml·min–1·100 ml–1·mmHg–1, 75 ± 16% of peak conductance) and strength-matched women (0.327 ± 0.11 ml·min–1·100 ml–1·mmHg–1, 74 ± 22% of peak conductance) at task failure (P = 0.95; Fig. 6C).

The 4-min contraction was 48% of the time to failure for the men and 47% for the women (P = 0.83). Although the contraction intensity and fatigue were similar at the end of the 4-min contraction, active hyperemia was greater for the men (34.7 ± 5.1 ml·min–1·100 ml–1, 86 ± 18% of peak flow) compared with the strength-matched women (26.9 ± 2.9 ml·min–1·100 ml–1, 64 ± 14% of peak flow; P = 0.038; Fig. 6B). Similarly, vascular conductance was greater for the men than the strength-matched women after the 4-min contraction (0.383 ± 0.20 ml·min–1·100 ml–1·mmHg–1, 80 ± 18% vs. 0.294 ± 0.10 ml·min–1·100 ml–1·mmHg–1, 57 ± 14% of peak conductance, P = 0.02; Fig. 6C).


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
ACKNOWLEDGMENTS
 REFERENCES
 
To understand the role of muscle perfusion in the sex differences of muscle fatigue for a submaximal sustained contraction, we compared the time to task failure, postcontraction (active) hyperemia, and vascular conductance for an isometric contraction performed by young men and women with the handgrip muscles. Because men are usually stronger than women and the absolute strength potentially influences the time to failure (22, 23), we examined active hyperemia and vascular conductance after brief and sustained isometric contractions when the men were stronger than the women (study 1) and when men and women were matched for strength (study 2). The main findings were that 1) the time to task failure was longer for the women compared with the stronger men, but it was similar when the men and women were matched for strength; 2) active hyperemia and vascular conductance were greater for the stronger men compared with the weaker women after brief submaximal contractions sustained between 20 and 80% of MVC force, but it was similar for those men and women who were matched for strength; 3) blood flow and vascular conductance were similar for the men and women at rest, after 10 min of occlusion, and at task failure for the fatiguing contraction sustained at 20% of MVC force when men were stronger than women and when the sexes were matched for strength; and 4) blood flow and vascular conductance were greater for the men than the women after the 4-min contraction when the men were stronger than the women and also when the men and women were matched for strength. Thus the sex difference in time to failure of a submaximal isometric fatiguing contraction was a function of the absolute strength exerted by men and women. Although absolute strength initially influenced the difference in active hyperemia and vascular conductance for an isometric contraction (brief contractions) of men and women, the sex difference in time to failure for sustained contractions was not dependent on active hyperemia and vascular conductance.

Sex Differences in Time to Task Failure are Dependent on the Absolute Strength

We found that when the men were stronger than the women, women were able to sustain the contraction at 20% of MVC force with the handgrip muscles for a longer duration than the men. Furthermore, there was an association with the absolute target force exerted such that those young adults who were stronger had a briefer time to failure (Fig. 1). This relation remained for the women when analyzed separately but not for the men, probably due to the reduced subject numbers and variability. However, the relative reduction in MVC force was similar for both sexes, indicating that the muscle fatigue experienced at termination of the task failure contraction was similar. Accordingly, both the men and women had maximal levels of perceived exertion at task failure indicating similar magnitudes of performance for the sexes. Consistent with these findings, we found that when the sexes were matched for handgrip strength, the time to task failure was similar for the men and women. Furthermore, regression analysis indicated that the most significant predictor of time to task failure was the strength of the subject. These results are consistent with previous findings for 1) strength-matched men and women of the elbow flexor muscles and plantar flexor muscles (16, 22) and 2) the associations observed for time to failure and the absolute force exerted by the elbow flexor muscles when young men were stronger than the women (21, 23, 25). Consequently, the sex difference in muscle fatigue for the sustained submaximal contraction with the arm muscles was a function of the strength of the men and women.

Because men are usually stronger than women, indirect evidence indicates (17, 23, 24) that women will experience less compressive force and intramuscular pressure in the muscle (2, 46, 48), allowing greater perfusion and oxygen supply compared with the men during the sustained contraction. To understand the hemodynamics during sustained contractions of men and women, we compared the active hyperemia and vascular conductance of men and women when men were stronger than women and when they were matched for strength for a sustained contraction performed at the same intensity of contraction.

Active Hyperemia and Vascular Conductance was Associated With Absolute Force for Brief Contractions in Men and Women

Active hyperemia and vascular conductance after the brief contractions increased with the increase in intensity between 20 and 80% of MVC force (Figs. 2 and 6A), as has been shown previously in strong vs. weak men (2). Consistent with our hypothesis, we observed that the active hyperemia and vascular conductance was greater for the stronger men compared with the women for the brief submaximal contractions at 20, 40, 60, and 80% of their maximal strength. When the men and women were matched for strength, vascular conductance and active hyperemia were similar for the sexes. Because perfusion of the muscle is inversely related to active hyperemia (56), these results indicate that, for these brief contractions, vessels of the women were less compressed and the muscle was more perfused compared with the stronger men who exerted greater absolute force during each of the brief contractions even though the relative force exerted for both sexes was similar.

Active Hyperemia and Vascular Conductance was Less for Women After 4 min of a Sustained Contraction

After 4 min of a sustained contraction, the hyperemia and vascular conductance was less for the women who exerted less absolute force than men (study 1). The women were at 70% of their peak flow and 58% of peak vascular conductance and the men at 99% of peak flow and 83% of peak conductance. Consequently, the weaker women experienced greater perfusion during the contraction when compared with the men at the same absolute time, which was 35% of the time to task failure of the women and 48% of time to failure for the men. Although there were associations with absolute strength for both the brief and sustained contractions, active hyperemia and vascular conductance measured after the 4-min sustained contraction were not fully explained by the absolute strength (and mechanical compression) exerted by the men and women. Contrary to expectations, when men and women were of similar strength, active hyperemia and vascular conductance was less for the women compared with the men at termination of the 4-min contraction. A 4-min contraction was 48 and 47% of the time to failure for strength-matched men and women, respectively, representing a similar absolute and relative time to failure and fatigue for the men and women. Although the time to failure was similar for the strength-matched men and women, active hyperemia and vascular conductance at 4 min were dissociated from the time to failure and therefore did not account for the time to failure for the fatiguing contraction in the men and women. These results were corroborated by the regression analysis that indicated the only significant predictors of time to task failure were the strength of the subject and the EMG activity at task failure. Consequently, the hyperemic response and vascular conductance were not significant predictors of time to task failure for the men and women. Therefore, strength alone and mechanical compression of vasculature do not explain the active hyperemia and vascular conductance after a sustained fatiguing contraction, as we observed for brief nonfatiguing contractions. Although the hyperemic response was initially dependent on strength of the isometric contraction, some other mechanism that is independent of strength influenced the magnitude of the active hyperemia and vascular conductance experienced after the sustained contraction in the men and women.

The sex difference in postcontraction blood flow was not explained by a difference in the increases in MAP because forearm vascular conductance differed similarly with that of active hyperemia for the men and women who differed in strength. Furthermore, the resting and peak levels of flow and conductance did not influence the sex differences in active hyperemia and vascular conductance because these did not differ between the men and women or across experimental days. Finally, there was no association between flow and conductance across the menstrual cycle for women for the active hyperemia after 4 min, after the submaximal contractions, or at rest or peak levels, indicating that the acute fluctuations in hormones over the menstrual cycle did not influence blood flow levels in the women at various times of their cycle.

The sex difference in flow and conductance at 4 min of the sustained contraction is likely due to a combination of 1) strength-associated differences in the intramuscular pressure and mechanical compression and kinking of vessels within the muscle (2, 31, 46, 48, 54) and the 2) the magnitude of vasoconstriction and/or vasodilation experienced in the working muscle. As a sustained contraction increases in duration, the intramuscular pressure will progressively increase (20, 46), and the muscle will become more ischemic. According to the results for the brief contractions, mechanical compression and intramuscular pressure may have had an initial influence on perfusion during the contraction. However, as the contraction was maintained, other mechanisms likely influenced the men and women differently. Vasodilation begins to occur on contraction (53, 54) and could have influenced the men and women similarly for the brief, nonfatiguing contractions but dissimilarly for the sustained contraction. During a sustained contraction, the metabolic by-products of muscle fatigue that are potential vasodilators of the muscle (10) may differ for men and women, possibly mediated by chronic exposure to sex hormones (19, 36), sex differences in metabolism (11, 28, 50, 51), or sex differences in fiber types, although this is still equivocal (29, 33, 38, 41, 49, 52). Furthermore, there are sex differences in sympathetic activation at rest and during static exercise (6, 12, 37), such that the magnitude of vasoconstriction is less for women than men. Consequently, sex differences in physiology that are independent of strength and mechanical compression of the feed arteries may contribute to the different hemodynamic responses of men and women during a sustained contraction, and these mechanisms warrant further investigation.

Active Hyperemia and Vascular Conductance Were Similar at Task Failure

At task failure, active hyperemia and vascular conductance were similar for the men and women in both studies. For an individual, active hyperemia will be greater for long-duration than for short-duration contractions (20, 32), as we observed for the women who reached peak levels of hyperemia by task failure but were only at 70% of the peak hyperemia after 4 min. The similar values at task failure suggest that those mechanisms contributing to the active hyperemia and vascular conductance had different time courses for the men and women, but both sexes had reached a similar physiological endpoint by task failure.

These results are consistent with the progressive increase in interference EMG that was similar at task failure for the men and women. During a submaximal contraction held to failure, motor unit recruitment progressively increases (4, 7, 13, 15, 35) as the already active muscle fibers fatigue and are not able to generate the required force. The increase in motor unit recruitment significantly contributes to the interference EMG that increased to similar levels at task failure for the men and women. These results suggest the proportion of the motor unit pool recruited at task failure was similar for the men and women. Accordingly, other indexes, including heart rate and perceived effort, that are indirect measures of central neural activity (5, 14, 18) indicated that the magnitude of neural activity was similar in the men and women at task failure.

In conclusion, the time to task failure for a submaximal contraction with the handgrip muscles was longer for young women compared with young men who were stronger but were similar for the sexes when matched for strength. For brief isometric contractions, active hyperemia and vascular conductance was dependent on the strength of the contraction and was greater in stronger men than women but similar when the sexes were matched for strength. For sustained fatiguing contractions, active hyperemia and vascular conductance were similar at task failure for men and women of all strength levels. However, when the contraction was sustained for the same absolute time and relative time, women had less active hyperemia and vascular conductance than the men after the 4-min contraction, even when matched for strength. Thus the sex difference in time to task failure for a sustained contraction of the finger flexor muscles was due to mechanisms associated with the absolute strength, but this did not involve differences in active hyperemia or vascular conductance. Future studies need to address those strength-associated mechanisms for the sex difference in muscle fatigue.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
REFERENCES
 
The authors thank the subjects and the following students who assisted with some of the data collection: Tiffany Trott and Tim Kufahl.


   FOOTNOTES
 

Address for reprint requests and other correspondence: S. K. Hunter, Exercise Science Program, Dept. of Physical Therapy, PO Box 1881, Marquette Univ., Milwaukee, WI 53201 (e-mail: Sandra.Hunter{at}marquette.edu)

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.


   REFERENCES
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 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 

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