Circulatory Response of Digital Arteries Associated with Electrical Stimulation of Calf Muscle in Healthy Subjects

HUEY-ING LIU, DEAN P. CURRIER, and A. JOSEPH THRELKELD

The purpose of this study was to investigate the effects of electrical stimulation (2,500-Hz sine wave modulated at 50 bursts per second) of the posterior calf musculature on the blood circulation of an unexercised part of the body, the ipsilateral digital arteries. Intensities of electrical stimulation sufficient to produce 15% and 30% of isometric maximum voluntary contraction (MVC) of the plantar flexor muscles were used. Twenty-four healthy subjects participated in this study and were assigned either to an Experimental Group receiving electrical stimula­tion (n = 13) or to a Control Group not receiving electrical stimulation (n = 11). Analysis of data revealed significant differences in finger blood flow when the calf musculature was stimulated electrically. We found significant differences in blood flow of the finger when torques produced by electrical stimulation of the calf musculature were raised to 15% and 30% of MVC. The results of the study indicate that blood flow in the ipsilateral finger decreases significantly when the posterior calf musculature is exercised artificially with electrical stimulation bursts. Key Words: Blood circulation, Electric stimulation, Physical therapy.

Voluntary exercise causes circulatory changes to occur in nonexercising parts of the body. Diversion of blood flow from the nonexercised parts of the body to volitionally exercised muscle is well established.1 Whether low frequency electrical stimulation (2,500-Hz sine wave modulated at 50 pulsed bursts per second) producing graded muscular responses af­fects blood flow of an unexercised part of the body is un­known.

Blair et al found a small increase in blood flow to the muscles of the forearm of untrained individuals who per­formed light exercises of the lower extremities, although blood flow to the skin of the forearm remained unchanged.2 Beve-gard and Shepherd reported a transient increase in forearm blood flow and a decrease in arterial blood pressure with the onset of lower extremity exercise. The forearm blood flow remained at the preexercise level during moderate volitional exercise, but blood flow decreased when heavy exercise was introduced.3 Zelis et al reported that in healthy subjects performing mild lower extremity exercise, forearm muscle blood flow did not change significantly, but with moderate and strenuous activity of the lower extremities, forearm blood flow was reduced significantly.4 In a recent study, Kitamura

et al demonstrated that finger blood flow decreased rapidly immediately after the onset of lower extremity exercise and remained at reduced levels throughout the exercise. Their results, however, indicated that the amount of decrease in finger blood flow during exercise was independent of exercise intensity.5

For some time, electrical stimulation of muscle has been used to study muscle metabolism and kinetics. Merton6 and Naess and Storm-Mathisen7 clearly demonstrated that the force elicited by maximum voluntary contractions (MVCs) and by electrical stimulation of muscles were the same. Rhythmic muscular contractions produced by electrical stim­ulation increase peripheral circulation in a fashion similar to voluntary contraction.

Wakim studied the influence of various frequencies of continuous direct electrical stimulation (4-256 Hz) on the blood flow in the stimulated extremity of the dog. He found that 16 pulses per second (pps) caused the greatest increase in blood flow to the exercised muscle, whereas higher frequencies (64, 128, and 256 Hz) resulted in much smaller increases in blood flow. Additionally, he reported that at various times during stimulation, the blood flow in the nonexercised leg increased, decreased, or was identical to the preexercise blood flow. He concluded, however, that electrical stimulation pro­duced an overall decrease in blood flow in the unstimulated extremity.8

Currier et al, using 2,500-Hz sine waves interrupted at 50 pulsed bursts per second that produced fused tetanic muscular contractions, reported an increase in blood flow to the stim­ulated muscle.9 This study represents results obtained from "new generation" electrical stimulators about which little is known concerning their effects on blood circulation. The

Ms. Liu is a staff physical therapist, Cardinal Hill Hospital 2050 Versailles Rd, Lexington, KY 40504. She was a graduate student at the University of Kentucky at the time this study was conducted.

Dr. Currier is Professor and Chairman, Department of Physical Therapy, HP500, University of Kentucky Medical Center, Lexington, KY 40536-0084 (USA).

Dr. Threlkeld is Assistant Professor, Department of Physical. Therapy, HP500, College of Allied Health Professions, University of Kentucky Medical Center.

This article was submitted October 23,1985; was with the authors for revision 15 weeks; and was accepted June 26, 1986. Potential Conflict of Interest: 4.

340 PHYSICAL THERAPY

RESEARCH electrical current characteristics of these stimulators have been promoted for augmenting muscular strength.1011

Electrical stimulation is being accepted clinically by physi­cal therapists as a means to increase the strength of healthy muscles. Most research on the effects of electrical stimulation on circulation, however, has not involved the type of state-of-the-art stimulator that we have used. The purpose of this study, therefore, was to investigate the effects of electrical stimulation (2,500 Hz modulated at 50 bursts per second) on the blood flow of an unexercised part of the body using current intensities sufficient to produce muscle contractions of 15% and 30% of MVC. We hypothesized that electrical stimulation of the right posterior calf muscle would not alter the circula­tion of the digital arteries in the ipsilateral long finger.

METHOD

Subjects Twenty-four healthy volunteer subjects (5 men, 19 women)

with normal heart rates and blood pressures, ranging in age from 20 to 28 years, participated in this study. All subjects signed an informed consent statement after being briefed on the purpose, procedures, and risks of the study. Subjects were assigned randomly to either the Experimental Group (n = 13) or the Control Group (n = 11). Table 1 gives the demographic information of these subjects.

Measurement of Ankle Torque The Experimental Group subjects were measured for MVC

of the plantar flexor musculature while the results were re­corded using an isokinetic dynamometer* interfaced with a multichannel graphic recorder† (damping set at 1). The Ex­perimental Group executed three isometric MVCs with a rest period of two minutes between trials. The highest torque value of the three contractions was used as the subjects' MVC. Torque measurements were obtained from all subjects who were positioned prone on a test table with their right foot secured to the lever arm of the dynamometer. The test leg was secured to the dynamometer at the foot (0° dorsiflexion) with webbed straps, and the knee was secured similarly to the table ensuring stability during the torque measuring proce­dure. The arms of the subjects were placed at their sides, and they were told not to use hand support during the MVC tests. The trunk was unsupported during exertion in order to min­imize assistance from body musculature other than the calf muscles. The dynamometer was set for 0°/sec to obtain an isometric torque reading.

Immediately after measuring the voluntary torque pro­duced by the calf musculature, we determined the current intensity required to produce electrically isometric torques equal to 15% and 30% of each Experimental Group subject's measured voluntary isometric MVC. We used these predeter­mined current intensities, specific to each Experimental Group subject, to induce isometric muscle contractions dur­ing the experimental procedure. Table 2 shows the group descriptive data of torque and current intensity determina­tions.

TABLE 1 Demographic Data of Subjects

Group

Control (n = 11)

Range s

Experimental (n = 13)

Range s

Age (yr)

25.6 20-30 3.2

25.8 20-36 6.0

Weight (kg)

57.9 51.4-68.2 5.6

62.9 48.8-77.3 10.6

Height (cm)

163.2 157.5-182.9

7.4

169.7 157.0-186.7

8.4

TABLE 2 Voluntary Maximum Isometric Torques and Current Intensities to Produce Percentages of Maximum Torque

Group

Control(n = 11)

Range s

Experimental (n =

Range s

= 13)

Active Isometric Torques (Nm)

72.0 50.1-109.8 16.8

59.1 32.5-89.4 15.6

Current Intensities (mA) to Produce Torques

15% MVC

11.8 9.5-17.0 2.5

30% MVC

15.5 12.0-25.0 4.0

Measurement of Heart Rate, Blood Pressure, and Finger Blood Flow

Subjects rested in a prone position on a treatment table for about 15 minutes while prestimulation preparations and re­cordings were made. Heart rate was measured by palpation of the right radial artery (pulse), and blood pressures were measured with a sphygmomanometer and auscultation of the right brachial artery. These baseline heart rates and blood pressures were obtained before MVC and percentage contrac­tions were determined. A second set of heart rate and blood pressure measurements was made at the conclusion of the experiment.

The blood flow of the ipsilateral third digital artery of each subject was assessed using a dual-frequency, continuous wave, ultrasonic directional Doppler device (Model 909,5.3 MHz).‡ The subjects' right arm was rotated laterally (externally) with the elbow slightly flexed, forearm pronated, and the hand and wrist maintained in a resting position. The Doppler signal was calibrated before the measurement sessions of the exper­iment. The room temperature was maintained at 22°C (72°F). The Doppler ultrasonic device was connected to the multi­channel graphic recorder to transcribe the blood flow signals of the artery. The pencil probe of the Doppler was positioned on the skin (coupled with conductive gel) over the volar surface of the third digit of the right hand (immediately distal to the metacarpal head) and moved to the angle and point at which the loudest, highest-pitched frequency shift from the

*Cybex, Div of Lumex, Inc, 2100 Smithtown Ave, Ronkonkoma, NY 11779. † Model R612, Beckman Instruments, Inc, 3900 River Rd, Schiller Park, IL

60176. ‡ Parks Medical Electronics, Inc, Beaverton, OR 97075.

Volume 67 / Number 3, March 1987 341

TABLE 3 Heart Rate and Blood Pressure Values Before and After Intervention

Group

Control (n = 11)

Range s

Experimental (n =

Range s

= 13)

Before

67.0 60-81 6.0

67.9 56-78 8.7

Heart Rate (bpm)

After

67.9 60-84 6.0

65.5 60-78 7.9

Blood Pressure Systollc/Diastollc

Before

105.6/65.6 102-120/54-84

5.8/9.3

107.1/69.1 98-120/58-80

7.0/8.7

(mm Hg)

After

102.9/64.5 100-116/56-78

5.5/7.2

105.8/66.7 100-128/56-84

7.7/8.2

artery was audible over the loudspeaker of the ultrasonic device. The probe position then was maintained by a clamp throughout the experiment. For each measurement, a tracing containing 20 to 25 consecutive analog signals (each repre­senting a complete cardiac cycle) was transcribed on the multichannel recorder. Doppler measurements were obtained in both groups during the prestimulation rest period (t = 0); at intervals of 1, 5, and 10 minutes between electrical stimu­lation cycles (t = 1,5, and 10); and at intervals of 1, 3, and 5 minutes after electrical stimulation was terminated (t = 11, 13, and 15).

Electrical Stimulation Procedure

An Electrostim 180-2§ stimulator provided the electrical stimuli to produce tetanic isometric contractions of the right calf musculature of the subjects in the Experimental Group. The stimulator produced individual sine waves at a frequency of 2,500 Hz in modulated bursts at a rate of 50 bursts per second. The timing sequence used in this study produced a 12-second output burst followed by an 8-second rest period (12:8 duty cycle). The bursts of stimuli had an intensity that was finely ramped (surged) so that peak voltage of each series of bursts increased gradually over a 2-second period and was sustained for 10 seconds. At the end of the 12-second stimu­lation period, the intensity declined abruptly and was followed by the 8-second rest period before the next stimulation cycle began.

One stimulator electrode (6.2 x 6.2 cm, flexible rubber) was placed over the motor point of the medial belly and a similar electrode was placed over the motor point of the lateral belly of the gastrocnemius muscle. The electrodes were secured to the lower leg by Velcro straps. The subjects were positioned prone with the ankle in neutral and the plantar surface of the foot stabilized against a rigid barrier. The first series of electrically induced isometric contractions and meas­urements were recorded at the predetermined intensity to produce 15% of MVC.

Electrical stimulation to the calf musculature was produced for a 10-minute period of time. A minimum 10-minute recovery period between experimental periods (or longer, if needed, after the last blood flow measurement) was imposed to allow digital blood flow to return to prestimulation resting levels. A second series of electrical stimulations and measure­ments was carried out using current intensities sufficient to

produce isometric torque equivalent to 30% of MVC. After completion of the 5-minute poststimulation (t = 15) blood flow measurement (30% MVC), heart rate and blood pressure measurements were obtained again.

Control Group subjects underwent conditions (position, electrode locations, and connections) and measurements (heart rate, blood pressures, finger blood flow, and torque) similar to those of the Experimental Group subjects but without electrical stimulation.

Data Analysis

We used the pulsatility index (PI) to analyze blood flow to the stimulated muscle. We calculated the PI using the follow­ing formula:

PI = PP/MD

where PP is the peak-to-peak signal size, and MD is the mean distance between signals averaged over several cardiac cycles.12 The mean peak amplitudes and mean cardiac cycle times (PP/MD) of each subject's centermost 15 cycles of 20 to 25 consecutive signals from each subject recorded at t = 0 to t = 15 were used in the analysis. Each PI value used in the blood flow analysis represents the mean of 15 analog signals recorded in each group of recorded signal tracings. A multi­variate analysis of variance (MANOVA)|| was used to exam­ine the group and time differences among the dependent variables (ie, heart rate, systolic blood pressure, and diastolic blood pressure) and the interaction differences between time (prestimulation, poststimulation) and group (Experimental, Control). A 2 (groups) x 2 (percentage of MVC) x 7 (meas­urement intervals) univariate ANOVA for repeated measures11 using each subject's PI as the dependent variable served to assess the effects of electrical stimulation. The groups were Experimental and Control; the percentages of MVC were 15% and 30%; and the intervals of measurement were t = 0, 1, 5, 10, 11, 13, and 15 minutes. Mean prestimulation values between the Experimental and Control Groups were examined by an independent t test (two-tailed) to determine equality between groups. Analysis of the mean prestimulation (t = 0) heart rate, blood pressure, and PI values showed that the groups were matched similarly on these variables before experimental intervention. Thus, no adjustments were made in the statistical analyses. A 5% probability level for signifi­cance (p < .05) was applied for all statistical tests. When

§ Micromed Instruments, Inc, 225 Migneron, St. Laurent, Quebec, Canada H4T 1W8. || SAS Computer Program, SAS Institute, Inc, Cary, NC 27511.

342 PHYSICAL THERAPY

RESEARCH TABLE 4 Multivariate Analysis Results

Sources

Group (Experi­mental, Con­trol)

HRa

Error SBPb

Error DBPC

Error Time (prestimula-

tion, post-stimulation)

HR Error SBP Error DBP Error

Time x group HR Error SBP Error DBP Error

df

1 24

1 24

1 24

1 24

1 24

1 24

1 24

1 24

1 24

SS

0.17 2493.38

76.33 1652.92

23.56 3206.62

6.94 138.62

42.48 239.69

32.33 325.69

38.94 138.62

2.33 239.69

8.48 325.69

MS

0.17 103.89

76.33 68.87 23.56

133.61

6.94 5.78

42.48 9.99

32.33 13.57

38.94 5.78 2.33 9.99 8.48

13.57

F

0.00

1.11

0.18

1.20

4.25

2.38

6.74

0.23

0.62

P

NS

NS

NS

NS

NS

NS

.01

NS

NS

TABLE 5 Univariate Analysis of Variance for Repeated Measures

Source

Group (Experimental vs Control)

Condition (15% vs 30% MVC)

Time (7 intervals) Group x condition Group x time Condition x time Group x condition x

time Error TOTALS

df

1

1 6 1 6 6

6 308 335

SS

22.35

0.01 6.39 0.01 5.83 2.72

2.30 61.60

1.22

MS

22.35

0.01 1.07 0.01 0.97 0.45

0.38 0.20

F

111.75

0.05 5.35 0.06 4.85 2.25

1.90

P

.001

NS .001 NS

.001

.05

NS

significant differences were found, the Newman-Keuls test was applied to discern which means of a treatment array were significantly different.

RESULTS

We found no significant differences between the Experi­mental and Control Groups based on their mean prestimu-lation (t = 0) heart rate, blood pressure (systolic and diastolic), and PI values. Table 3 presents a summary of the prestimu-lation and poststimulation heart rate and blood pressure data.

Table 4 shows that heart rates and blood pressures were unaffected between the Experimental and Control Groups, between the designated prestimulation and poststimulation time periods, and within the time-by-group interaction. The one exception among the nonsignificant dependent variables

from the multivariate analysis was the statistically significant time-by-group interaction for heart rate.

Blood flow data of this study are presented in Table 5 and Figures 1 through 3. Findings show that the independent variables of group (Experimental Group vs Control Group) and time (specific measurement intervals) had significant influence on the outcomes of this study. Electrically induced contractions of calf musculature were effective in altering blood flow in the third digital artery of the ipsilateral upper extremity in the Experimental Group compared with the Control Group. That is, in the Experimental Group, the Neuman-Keuls test indicated that the mean PIs decreased significantly at intervals of 1, 5, and 10 minutes (t = 1, 5, and 10) during the stimulation period producing torques equal to both 15% and 30% of MVC (Figs. 1, 2). No statistical differ­ences in mean PIs occurred between experimental conditions of 15% or 30% of MVC (Figs. 1, 2). No statistical differences in mean PIs occurred between experimental conditions of 15% or 30% of MVC except at intervals t = 5 and 15 minutes (Fig. 3). No significant differences in mean PIs were revealed between the Experimental and Control Groups at intervals t = 0, 10, 11, or 13 minutes.

DISCUSSION

The experiment had no significant effect on the blood pressures of the subjects. Electrical stimulation to the calf musculature of one leg did not influence either the systolic or diastolic blood pressures of the Experimental Group subjects. Significant time-by-group interaction for heart rate implies that some subjects in the Experimental Group had decreased heart rates throughout the experiment. Because the heart rates of the Experimental and Control Groups were statistically equal before the intervention, the reduction of heart rate in the Experimental Group subjects could be attributed to their reduced anxiety about the electrical stimulation experience. Because the change in heart rate was not accompanied by blood pressure fluctuations, the affected heart rate may be due to chance rather than anxiety. A change in heart rate also was observed in another study of electrical stimulation on blood flow.9

The main effects and those of interaction appear to be significantly related in this study. The poststimulation (t = 11-15) digital blood flow of the Experimental Group's nonex-ercised extremities returned to the prestimulation (t = 0) level after a stimulus intensity of 15% of MVC, but with a stimulus intensity of 30% of MVC the blood flow remained increased at five minutes poststimulation (t = 15). This observation of blood flow behavior in the digital artery of a nonexercised extremity differs from that reported previously for blood flow behavior to the muscle being stimulated electrically.9 In the electrically stimulated muscle, no significant increase in post-stimulation blood flow was reported,8 although in our study the stimulus intensity of 30% of MVC resulted in a rapid increase in blood flow during the 3- to 5-minute poststimu­lation (t = 13 and 15) intervals. The data of our study imply that the electrical stimulation intensity may affect the blood flow of the ipsilateral nonexercised extremity. This finding of graded stimulus intensity influencing the blood flow of the ipsilateral nonexercised extremity agrees with the work of Littell.13

Our finding of a sudden drop in finger blood flow during the first minute of muscle contractions at both the 15% and 30% of MVC contraction levels is in agreement with the

a Heart rate. b Systolic blood pressure. c Diastolic blood pressure.

Volume 67 / Number 3, March 1987 343

Fig. 1. Mean and standard deviation of pulsatility indexes (PIs) in the third digital artery during prestimulation, stimulation, and poststim-ulation intervals of the plantar flexor muscles at current intensities producing isometric torque equivalent to 15% of MVC for the Exper­imental Group. The nonstimulated Control Group's mean PIs are plotted for comparison. Pulsatility index is the ratio of peak-to-peak pulse amplitude divided by mean distance between 15 pulse cycles.

Fig. 2. Mean and standard deviation of pulsatility indexes (PIs) in the third digital artery during prestimulation, stimulation, and poststim-ulation intervals of the plantar flexor muscles at a stimulation intensity sufficient to elicit isometric torque of 30% of MVC for the Experimental Group. The nonstimulated Control Group's mean PIs are plotted for comparison.

Fig. 3. Mean and standard deviation of pulsatility indexes in the third digital artery during prestimulation, stimulation, and poststimu-lation intervals. The responses to both 15% and 30% of MVC of the plantar flexor muscles in the Experimental Group are plotted.

results of others. Kitamura et al reported that finger blood flow decreased rapidly immediately after the onset of voli­tional exercise of the lower extremity and throughout the exercise.5 Blair et al, measuring forearm blood flow during leg exercise, demonstrated an increase in vascular tone of the forearm vessels that was proportional to the intensity of the exercise. The vasoconstriction was attributed to sympathetic fibers supplying the vasculature.2 Bishop et al14 and Muth et al,15 in contrast, reported no change in blood flow to inactive muscles during volitional exercise, but Muth et al suggested that muscle blood flow might decrease with more stressful exercise. Zelis et al reported that forearm muscle blood flow decreased significantly during moderate and strenuous inten­sities of leg exercise.4 Based on this evidence, vasoconstriction appears to be mediated by the sympathetic nervous system and occurs in the nonexercised limbs after minimal exercise of an isolated body part. Wallin et al could not correlate nerve activity with vasodilatation,16 which supports studies that cite sympathetic vasoconstrictors as the major regulatory agents of blood flow in nonexercised muscles during exercise.17,18

Littell analyzed the behavior of vasoconstrictor muscle fibers at the beginning and end of exercise and concluded that increases in activity of the sympathetic vasoconstrictor fibers of nonexercised muscles are the result of peripheral stimuli (reflex responses to exercise) rather than of concurrent cortical activation of the sympathetic system and skeletal muscles.13

The increase in sympathetic vasoconstrictor activity results in a graded decrease in blood flow to the inactive muscles proportional to the work load. This sympathetic nervous system activity shunts part of the cardiac output to the active muscles and skin circulation. The need to dissipate the excess heat generated by the increased metabolic activity of the exercised muscles causes the increase in skin blood flow.2,3,14,15

The vasodilatation of the exercised region is thought to be caused by sensitivity of the vessels to locally accumulated metabolites.19 This vasodilatation effect appears to be inde­pendent of sympathetic activity. This independence was dem­onstrated by Remensnyder et al who found that vessels in the active muscles of dogs were relatively immune to sympathetic stimulation.20

In the vessels of the hand, response to exercise is a balance between a reflex increase in constrictor muscle tone secondary to the exercise and a reflex decrease in constrictor muscle tone caused by the rise in body temperature.21 At the onset of exercise, vasoconstriction predominates and blood flow to the hand decreases. As exercise continues, the blood flow to the hand increases but still is opposed by the reflex constriction induced by the exercise. Numerous researchers have found that blood flow to the hand decreases during leg exer­cise.2"51415 A similar observation was found in our study between the Experimental and Control Groups that exhibited no significant difference during prestimulation, stimulation, and poststimulation periods. Considerable variation exists between the methodology of our investigation using electri­cally induced contractions versus other studies that used voluntary muscle contractions. Most studies used bicycle ergometers to exercise the entire leg, whereas our study in­volved only the calf musculature. Although the percentage of MVC isometric torque elicited by voluntary contraction and by electrical stimulation of muscle is the same, physiological changes such as altered heart rate and blood pressure associ­ated with voluntary exercise6,7 were not observed in our Ex­perimental Group. Further research is needed to determine whether voluntary exercise and exercise by electrical stimu-

344 PHYSICAL THERAPY

RESEARCH lation of equal torque production affect skin blood flow similarly.

Electrical stimulation has been used to reduce circulatory stasis to prevent venous thrombosis and pulmonary em­bolus.22 Electrical stimulation is used often in the manage­ment of soft tissue injuries in which increased blood flow is desirable.8,9 In either condition, the physical therapist applies the electrical stimulation to the involved muscle to improve local circulation. Although the blood flow to the stimulated muscle may increase, the results of this study suggest that the increased local circulation appears to be at the expense of circulation elsewhere in the body. Physical therapists should be aware that the electrically induced form of exercise may have remote circulatory effects similar to those produced by volitional exercise.

Physical therapists also should be aware that activation of the calf musculature does not appear to alter the heart rate and blood flow pressures of subjects receiving low intensity electrical stimulation. Because the absence of exercise-induced

vasoconstriction has been reported to limit the volume of blood available to support the increased cardiac output re­quired during exercise13 and because electrical stimulation simulates voluntary exercise by altering blood flow, caution should be observed with patients with impaired innervation of peripheral vasculature.

CONCLUSIONS

Electrical stimulation having current characteristics of 2,500-Hz sine waves modulated at 50 bursts per second at an intensity sufficient to produce 15% or 30% of isometric MVC torque of the calf musculature of one leg produces a decrease in finger blood flow in the ipsilateral hand and decreases the blood flow in the artery of the third digit within the first minute of electrical stimulation. Finally, blood flow remains below the resting level of flow throughout the interval in which isometric muscle contractions equal to 15% and 30% of MVC are produced by electrical stimulation.

REFERENCES 1. Astrand P-O, Rodahl K: Textbook of Work Physiology: Physiological Bases

of Exercise, ed 2. New York, NY, McGraw-Hill Book Co, 1977, pp 170-176

2. Blair DA, Glover WE, Roddie IC: Vasomotor responses in the human arm during leg exercise. Circ Res 9:264-274, 1961

3. Bevegard BS, Shepherd JT: Reaction in man of resistance and capacity vessels in forearm and hand to leg exercise. J Appl Physiol 21:123-132, 1966

4. Zelis R, Mason DT, Braunwald E: Partition of blood flow to the cutaneous and muscular beds of the forearm at rest and during leg exercise in normal subjects and in patients with heart failure. Circ Res 24:799-806, 1969

5. Kitamura K, Hangyo K, Yamaji K: Finger blood flow decrease in leg exercise. Jpn J Physiol 32:141-144, 1981

6. Merton PA: Voluntary strength and fatigue. J Physiol (Lond) 123:553-564, 1954

7. Naess K, Storm-Mathisen A: Fatigue of sustained contractions. Acta Physiol Scand 34:351-366, 1955

8. Wakim KG: Influence of frequency of muscle stimulation on circulation in the stimulated extremity. Arch Phys Med 34:291-295, 1953

9. Currier DP, Petrilli CR, Threlkeld AJ: Effect of graded electrical stimulation on blood flow to healthy muscle. Phys Ther 66:937-943, 1986

10. Kramer JF, Mendryk SW: Electrical stimulation as a strength improvement technique: A review. Journal of Orthopaedic and Sports Physical Therapy 4:91-98, 1982

11. Currier DP, Mann R: Muscular strength development by electrical stimu­lation in healthy individuals. Phys Ther 63:915-921, 1983

12. Skidmore R, Woodcock JP, Wells PNT, et al: Physiological interpretation of Doppler-shift waveforms: 3. Ultrasound Med Biol 6:227-231, 1980

13. Littell EH: Neural regulation of blood flow in nonworking muscles: Part 3. Phys Ther 61:1575-1584, 1981

14. Bishop JM, Donald KW, Taylor SH, et al: Blood flow in the human during supine leg exercise. J Physiol (Lond) 137:294-308, 1957

15. Muth HAV, Wormald PN, Bishop JM, et al: Further studies of blood flow in the resting arm during supine leg exercise. Clin Sci 17:603-610, 1958

16. Wallin BG, Sundlöf G, Delius W: The effect of carotid sinus nerve stimula­tion on muscle and skin nerve sympathetic activity in man. Pflugers Arch 358:101-110,1975

17. Eklund B, Kaijser L, Knutsson E: Blood flow in resting (contralateral) arm and leg during isometric contraction. J Physiol (Lond) 240:111-124, 1974

18. Delius W, Hagbarth K-E, Hongell A, et al: General characteristics of sympathetic activity in human muscle nerves. Acta Physiol Scand 84:65-81,1972

19. Milnor WR: The circulation. In Mountcastle VB (ed): Medical Physiology, ed 13. St. Louis, MO, C V Mosby Co, 1974, vol 2, pp 938-940, 955

20. Remensnyder JP, Mitchell JH, Sarnoff SJ: Functional sympatholoysis during muscular activity: Observations on influence of carotid sinus on oxygen uptake. Circ Res 11:370-380, 1962

21. Gaskell P: Are there sympathetic vasodilator nerves to the vessels of the hands? J Physiol (Lond) 131:647-656, 1956

22. Apperly FL, Cary MK: The control of circulatory stasis by the electrical stimulation of large muscle groups. Am J Med Sci 216:403-406, 1948

Volume 67 / Number 3, March 1987 345