Circulatory Responses to Voluntary and Electrically Induced Muscle Contractions in Humans.

Key Words: Exercise, Regional blood flow, Transcutaneous electrical nerve stimulation.

The beneficial effects of transcutaneous electrical nerve stimulation (TENS) on limb blood flow in patients with circulatory deficits have been described in some case reports.[1,2] In experimental animals and humans with no known pathology, TENS has been shown to increase regional blood flow; however, the preponderance of evidence indicates that it does so only at stimulation intensities sufficient to cause skeletal muscle contraction.[3-10] Whether the increased blood flow found in these previous studies resulted from the TENS or from the skeletal muscle contraction produced by the TENS is unknown. It is also unclear whether electrically evoked muscle contractions offer a therapeutic advantage over voluntary contractions in terms of their ability to effect circulatory changes in the clinical setting.

In 2 studies,[6,11] the circulatory responses to electrically evoked and voluntary muscle contractions in humans with no known pathology were compared. Walker et al[11] studied the effects on blood flow of electrically evoked versus voluntary contractions of the calf muscles. Isometric calf muscle contractions at 10% and 30% of the subjects' maximal force output were electrically induced. In another protocol in the same study, voluntary contractions were produced in a rhythmic manner at the same relative workloads. The authors found that voluntary muscle contractions produced increases in popliteal artery blood flow, whereas electrically evoked contractions did not. The meaning of this difference is unclear, however, because of the nonuniform exercise modes used in the 2 protocols (ie, sustained electrically induced contractions versus intermittent voluntary contractions). Sustained and intermittent muscle contractions are known to produce different effects on blood flow.[12-14]

In the other study, Kim et al[6] examined blood flow in response to electrically evoked and voluntary contractions of the quadriceps femoris muscles during onelegged exercise. Rhythmic contractions were electrically evoked at the rate of 50 Hz using electrodes positioned over the vastus medialis and vastus lateralis muscles. In another protocol used in the same study, the subjects voluntarily extended their knees at the same work rates, duty cycles, and exercise bout durations. The authors found that peak muscle blood flow was the same during voluntary and electrically induced contractions. It is not clear, however, whether the active muscle mass was the same in the 2 protocols (the entire quadriceps femoris muscle during voluntary contractions versus only the vastus muscles during electrically induced contractions). The size of the active muscle mass is likely to be an important determinant of blood flow because of the tight coupling known to exist between blood flow and metabolic rate.[15]

Because of difficulties in the interpretation of these previous findings, the question of whether electrically evoked and voluntary contractions elicit similar increases in blood flow remains unanswered. The purpose of this study, therefore, was to compare circulatory responses to electrically induced and voluntary calf muscle contractions performed with the same force output, duty cycle, and active muscle mass.

Method

Subjects

Seven men and 7 women (mean age=28 years, SD=8, range=18-49) served as subjects. All subjects, by selfreport, were nonsmokers, were receiving no medications, and had no history of neuromuscular or cardiovascular disease. All subjects provided informed consent.

General Procedures

Subjects were studied in the supine position in a temperature-controlled (24 [degrees]-25 [degrees] C) laboratory (Fig. 1). The subjects participated in 2 testing sessions: 1 session to become familiar with TENS and the test environment and 1 session for measurement of responses. Three subjects were tested an additional time to evaluate reproducibility of responses. Blood pressure was measured using a Dinamap 1846 SX/P automated sphygmomanometer.(*) Heart rate was measured from the electrocardiogram. Calf blood flow was measured by venous occlusion plethysmography (model 271 plethysmograph([dagger])). Details concerning the methods, rationale, and assumptions for venous occlusion plethysmography have been published previously.[16-18] The reliability of our plethysmographic and sphygmomanometric measurements was assessed by calculating the coefficients of variation (standard deviation/mean x 100) for repeated measurements made under baseline conditions. The mean values for all subjects' coefficients of variation were 6.2% for blood flow measurements and 2.3% for blood pressure measurements.

[Figure 1 ILLUSTRATION OMITTED]

Electrical Stimulation

A Theratouch 7.7 point stimulator([double dagger]) was used to map the course of the tibial nerve in the popliteal fossa. A 20.3-[cm.sup.2] stimulating electrode (Empi series 9000 ([sections]) was then placed over the tibial nerve at the point where maximal plantar flexion of the foot was elicited without concomitant contraction of the peroneus longus or tibialis anterior muscle. A 20.3-[cm.sup.2] dispersive electrode([sections]) was placed on the medial belly of the gastrocnemius muscle. A sinusoidal waveform with a carrier frequency of 2,500 Hz and burst frequency of 20 Hz was used. This burst frequency was chosen because it is within the reported optimal range for increasing blood flow.[7,10] Stimulation intensity was set at a level that elicited the strongest plantar-flexor contraction that could be tolerated by each subject in a series of intermittent contractions with a duty cycle of 4 seconds "on" and 4 seconds "off" (minimum force output=68 N).

Force Measurements

Plantar-flexion force was measured using an elevated footplate coupled to a force transducer (model 13/2443-08([parallel])) that was mounted 18 cm distal to the subject's heel (Fig. 1). The subject's foot was strapped to the footplate, and the footplate was pivoted at the ankle joint so that the measured force was proportional to ankle torque. The force transducer was calibrated over the range of 0 to 225 N before and after each testing session by static weight loading. Output from the force transducer was amplified (Heath Kit amplifier(#)), recorded on paper and on magnetic tape, and directed to an oscilloscope so that the subject received visual feedback on force generated with each contraction.

Electromyographic Recordings

To ensure that the same amount of muscle mass was activated during voluntary and electrically evoked contractions, integrated electromyographic (EMG) activity of the peroneus longus and tibialis anterior muscles was recorded (AT 33 electromyograph(**)). We were concerned that the peroneus longus muscle, a plantar flexor not innervated by the tibial nerve, might contribute to the force output during voluntary contractions but not electrically evoked contractions, thereby creating a disparity in the size of the active muscle mass in the 2 protocols. We were also concerned that the tibialis anterior muscle might co-contract with the plantar flexors during voluntary exercise as the subject attempted to match the target force. To guard against these possibilities, the subject was instructed to keep contractions of these muscles to a minimum during the voluntary exercise protocol, and we monitored the EMG activity of the muscles to ensure adherence to this instruction. The subject was given muscle-specific audio feedback of the EMG activity for the 2 muscles, with the sensitivities set so that the subject was aware of very small ([is less than] 10% maximal) contractions.

All measurements except blood pressure were recorded on a paper chart recorder (model TA4000([dagger]) ([dagger]). In addition, analog signals were digitized (model 3000A PCM recording adapter([double dagger])([double dagger])) and saved on magnetic tape (model HR-D860U videocassette recorder([subsections])). The electrocardiographic and force output signals were digitized at a rate of 128 Hz with a 12-bit resolution and saved on computer disk for subsequent off-line analysis.

Exercise Protocols

During the TENS protocol, a cycle of 4 seconds "on," with a 2-second ramp up to maximum intensity, and 4 seconds "off" was used. During the voluntary exercise protocol, the subject was instructed to mimic the electrically evoked contractions as closely as possible. A metronome was used to cue the subject regarding the specified duty cycle, and an oscilloscope provided visual feedback regarding the target force level. The subject avoided peroneus longus and tibialis anterior muscle contractions by minimizing the audio EMG feedback from these muscles. During a 5-minute baseline data collection period (no exercise), calf blood flow was measured every 15 seconds. The first exercise protocol (either voluntary or TENS, order randomly determined) was then performed for 10 minutes. The intermittent contractions were interrupted for 25 seconds every 2 minutes for 2 blood flow measurements (1 measurement done immediately after the cessation of contractions and 1 measurement done 15 seconds after the cessation of contractions). During a 5-minute recovery period, blood flow was measured every 15 seconds. Heart rate and blood pressure were measured at 1-minute intervals during the baseline, exercise, and recovery periods.

Data Analysis

Force was analyzed by integration of the area under the force-versus-time curve. The sum of all the force integrals for the entire exercise protocol was determined as well as the average force per contraction. Trials in which the force outputs during voluntary and electrically induced contractions differed by more than 15% were excluded from analysis. The EMG activity recorded from the peroneus longus and tibialis anterior muscles during the voluntary exercise protocol was expressed as a percentage of the activity recorded previously during a maximal voluntary contraction.

Blood flow measurements made during the exercise protocols were grouped according to whether they were obtained immediately following the 2-minute series of contractions or 15 seconds after the cessation of contractions. The group mean values for immediately postexercise blood flow values for the 5 exercise bouts within each protocol were compared by analysis of variance to detect any differences in blood flow responses over time. This procedure was repeated for the 15-second postexercise values. Because there were no differences over time (P [is greater than] .05), the data from the 5 exercise bouts within each exercise protocol were averaged so that each subject had one value for the immediate postexercise measure and one value for the 15-second postexercise measure.

Hemodynamic variables (blood flow, vascular resistance, heart rate, and mean arterial pressure) measured at 3 time points (baseline, immediately postexercise, and 15 seconds postexercise) during voluntary and electrically induced contractions were compared by a 2-way (time x exercise protocol) ANOVA for repeated measures on the time factor. When the overall F test for time or for time X condition (voluntary or electrically induced contractions) interaction was statistically significant, paired t tests with Bonferroni corrections for multiple comparisons were used to detect differences among means.

Time to recovery was defined as the time required for the cardiovascular variables to return to within the 95% confidence interval of the baseline values. Paired t tests were used to compare times to recovery of hemodynamic variables and to compare force outputs in the voluntary and TENS protocols. Except where otherwise noted in the text and figures, data are presented as means ([+ or -] standard error of the mean). Probability values of less than .05 were considered statistically significant.

Results

Baseline Values

Measurements of calf blood flow, calf vascular resistance, mean arterial pressure, and heart rate were similar in the baseline periods before the voluntary and TENS protocols (Table).

Table. Mean ([+ or -] SEM) Hemodynamic Responses to Voluntary and Electrically Evoked Muscle Contractions

                                        Baseline

Calf blood flow (mL/100 mL/min)
  Voluntary                         4.7 [+ or -] 0.2
  Electrically evoked               4.5 [+ or -] 0.1

Calf vascular resistance
 (arbitrary units)
  Voluntary                        22.7 [+ or -] 1.1
  Electrically evoked              22.8 [+ or -] 0.8

Mean arterial pressure (mm Hg)
  Voluntary                          82 [+ or -] 2
  Electrically evoked                83 [+ or -] 2

Heart rate (bpm)
  Voluntary                          62 [+ or -] 3
  Electrically evoked                62 [+ or -] 3

                                        Immediately
                                        Postexercise

Calf blood flow (mL/100 mL/min)
  Voluntary                         10.3 [+ or -] 0.3
  Electrically evoked               11.1 [+ or -] 0.3(a)

Calf vascular resistance
 (arbitrary units)
  Voluntary                         10.3 [+ or -] 0.5(a)
  Electrically evoked                9.1 [+ or -] 0.3(a)

Mean arterial pressure (mm Hg)
  Voluntary                           85 [+ or -] 2
  Electrically evoked                 83 [+ or -] 2

Heart rate (bpm)
  Voluntary                           65 [+ or -] 3
  Electrically evoked                 64 [+ or -] 3

                                    15 s Postexercise

Calf blood flow (mL/100 mL/min)
  Voluntary                         5.9 [+ or -] 0.7
  Electrically evoked               6.9 [+ or -] 0.2(a)

Calf vascular resistance
 (arbitrary units)
  Voluntary                        18.3 [+ or -] 0.9
  Electrically evoked              14.0 [+ or -] 0.5(a)

Mean arterial pressure (mm Hg)
  Voluntary                          84 [+ or -] 2
  Electrically evoked                83 [+ or -] 2

Heart rate (bpm)
  Voluntary                          65 [+ or -] 3
  Electrically evoked                64 [+ or -] 3

(a) P <.05, postexercise versus baseline, 2-way repeated-measures analysis of variance (df = 2).

Force

The average force integral per contraction was comparable for the voluntary and TENS protocols (365 [+ or -] 27 versus 355 [+ or -] 27 N.s). Likewise, the total force integral for the voluntary and TENS protocols was similar (29,106 [+ or -] 2,146 versus 28,939 [+ or -] 2,264 N.s, P [is greater than] .05). The average EMG activity for the peroneus longus muscle was 7% [+ or -] 2% of that elicited during the subjects' maximal voluntary contractions. Analysis of EMG activity of the tibialis anterior muscle performed for 10 of the 14 subjects revealed an average value of less than 1% of maximal voluntary contraction.

Effects of Voluntary and Electrically Evoked Contractions on Hemodynamic Variables

The group mean values for calf blood flow and vascular resistance during the 2 exercise protocols are shown in Figure 2. The Table and Figure 3 show that both voluntary and electrically evoked contractions caused an increase in calf blood flow and a decrease in calf vascular resistance that were evident in the immediate postexercise measurements. The increase in blood flow and decrease in vascular resistance persisted until the 15-second postexercise measurements during the TENS protocol only. There was no time X condition interaction for either blood flow or vascular resistance. Times to recovery for calf blood flow (84 [+ or -] 75 versus 138 [+ or -] 105 seconds) and vascular resistance (86 [+ or -] 74 versus 118 [+ or -] 94 seconds) were comparable in the voluntary and TENS protocols (Fig. 4). Neither exercise protocol elicited changes in heart rate or mean arterial pressure (Table).

[Figures 2-4 ILLUSTRATION OMITTED]

We examined day-to-day variability of responses in 3 subjects. The immediate postexercise increases in calf blood flow, relative to the baseline measurements, were 137% on day 1 and 149% on day 2 for the voluntary exercise protocol and 230% on day 1 and 191% on day 2 for the TENS protocol. The respective values for the 15-second postexercise increases in blood flow were 29% and 38% for the voluntary exercise protocol and 72% and 81% for the TENS protocol.

Discussion

We compared the hemodynamic responses to voluntary and electrically induced contraction protocols that were comparable in terms of duty cycle, force, and active muscle mass. The major finding is that the 2 modes of exercise caused increases in blood flow and decreases in calf vascular resistance that were similar in magnitude but different in duration. Both exercise protocols caused increases in blood flow and decreases in vascular resistance that were evident immediately postexercise. Only electrically evoked contractions, however, produced vasodilation that was maintained above baseline levels for 15 seconds postexercise. The group mean values for blood flow recovery time were the same with both protocols; nevertheless, recovery times were longer after electrically induced contractions in 10 of the 14 subjects. In this regard, it is important to note that the statistical power associated with this particular t test was low (33%), probably due to the size of the intersubject variability relative to the size of the physiologic effect.

Critique of Methods

The strain gauge used to register limb circumference during venous occlusion plethysmography is very sensitive to movement artifact; therefore, this technique cannot be used to measure blood flow during muscle contraction. Nevertheless, because the postexercise measurements were initiated immediately after relaxation (within 1 second), we contend that these blood flow measurements closely approximate the undisturbed flow rate immediately prior to venous occlusion, that is, during exercise.[16]

Venous occlusion plethysmography measures blood flow in the entire limb; therefore, separate measurements of blood flow to muscle and to skin cannot be obtained using this technique. On the basis of our data, we cannot determine whether the exercise-induced increases in blood flow occurred primarily in muscle, skin, or both vascular beds. We consider it unlikely, however, that changes in skin blood flow contributed importantly to the observed changes in limb blood flow. The room temperature was controlled at 24 [degrees] C, and potential distractions inherent in the laboratory environment were kept to a minimum. Thus, fluctuations in skin blood flow caused by thermoregulatory and arousal responses were minimized.[19]

We considered the possibility that the active muscle mass was larger during voluntary contractions than during electrically evoked contractions and that this factor influenced our results. None of our subjects were able to totally relax the peroneus longus muscle (a plantar flexor muscle not innervated by the tibial nerve) during voluntary contractions. The peroneus longus muscle EMG activity recorded during voluntary contractions was on average 7% of that recorded during maximal contractions, indicating that this muscle contributed to the force in a small, but potentially important, way. If so, similar increases in blood flow despite a smaller active muscle mass would suggest that TENS is actually more effective than voluntary exercise in increasing blood flow.

Hemodynamic Responses to Voluntary Versus Electrically Evoked Contractions

In our subjects, voluntary and electrically evoked contractions of the calf muscles produced nearly identical increases in calf blood flow. Our findings agree with those of previous investigators[6] who found that voluntary and electrically evoked contractions of the quadriceps femoris muscle increased leg blood flow by comparable amounts. The findings of our study are consistent with those of the previous study despite the fact that different exercise protocols were used. Kim et al[6] observed blood flow response to isotonic contractions of a large muscle mass, whereas we studied blood flow responses to isometric contractions of a relatively small muscle mass. In the previous study, the size of the active muscle mass may not have been identical during the TENS and voluntary protocols (vastus muscles versus entire quadriceps femoris muscle). Nevertheless, the metabolic rates were probably comparable because the workloads were well matched.

In contrast, our findings do not agree with those of Walker et al,[11] who found that voluntary contractions increased blood flow to a greater extent than did electrically evoked contractions. In their study, however, direct comparison of blood flow changes elicited by electrically evoked and voluntary contractions is not possible because sustained muscle contractions were used in the TENS protocol and intermittent contractions were used in the voluntary exercise protocol. It is well known that sustained and intermittent contractions have widely dissimilar hemodynamic effects.[12-14] In addition, Walker et al[11] did not ensure that the same muscle mass was active in the 2 protocols. It is possible that the peroneus longus and soleus muscles were activated along with the gastrocnemius muscle during the voluntary exercise protocol, whereas only the gastrocnemius muscle was active during the TENS protocol. Thus, blood flow may have increased more in the voluntary exercise protocol because of the larger active muscle mass and resultant higher metabolic rate.

Mechanism of the Hemodynamic Changes Caused by Voluntary and Electrically Evoked Contractions

Because we did not observe systemic cardiovascular responses to either form of exercise (heart rate and blood pressure did not change), we assume that the exercise-induced reductions in calf vascular resistance were caused mainly by local mechanisms. The "muscle pump"[20,21] and flow-induced vasodilation produced by local release of endothelial-derived relaxing factors[22,23] are potential mechanisms for the observed vasodilation.

What mechanism explains the slightly longer persistence of the vasodilation produced by TENS versus voluntary exercise? We speculate that this difference may be secondary to a basic qualitative difference in electrically evoked versus voluntary muscle contractions. In electrically evoked contractions, there is at least a partial reversal in the order in which motor units are recruited (a large-to-small, as opposed to a small-to-large, order in voluntary contractions),[24,25] and motor units fire synchronously with electrically induced contractions as opposed to asynchronously with voluntary contractions.[26-29] Reversal of the recruitment order during TENS would be expected to alter the proportion of type I versus type II muscle fibers participating in the contraction. Recruitment of more type II fibers during TENS could lead to an increase in the release of vasodilatory metabolites such as hydrogen ion, adenosine, or phosphate.[30-32] Previous investigators[33] have observed that leg oxygen consumption is higher during electrically induced versus voluntary exercise at a given work rate, which suggests that TENS elicits a less efficient contraction. In addition, the shorter-lived vasodilation observed after voluntary exercise could have been caused, at least in part, by a neural mechanism. "Central command," the activation of medullary cardiovascular neurons in parallel with activation of alpha motoneurons, operative during voluntary exercise but not during electrically induced exercise, may have caused increases in sympathetic outflow to skeletal muscle or skin.[34,35] In summary, we demonstrated that voluntary and electrically evoked muscle contractions involving the same force, duty cycle, and active muscle mass produced vasodilatory responses that were nearly identical in magnitude. The vasodilation produced by the electrically induced contractions had a slightly longer duration than that produced by voluntary contractions; however, the circulatory effects of both modes of exercise were very short-lived ([is less than] 1 minute).

Conclusion

Physical therapy textbooks describe beneficial effects of TENS on regional blood flow.[36,37] Nevertheless, our study demonstrated that TENS applied using stimulation characteristics that are reportedly optimal for increasing blood flow is no more effective than voluntary exercise at matched force output and duty cycle. These findings suggest that the muscle contraction, rather than the stimulation, by itself, is responsible for the vasodilatory effect of TENS. Therefore, it is unlikely that TENS offers a therapeutic advantage over voluntary exercise in effecting short-term circulatory improvements, at least in patients with intact motor control systems. This may not be the case, however, in patients who are unable to perform voluntary exercise secondary to neuromuscular dysfunction.

(*) Critikon Inc, PO Box 31800, Tampa, FL 33631.

([dagger]) Parks Medical Electronics Inc, Box 5669, Aloha, OR 97006.

([double dagger] Rich-Mar Corp, Rte 3, Box 879, Inola, OK 74036.

([sections]) Empi Inc, 5999 Cardigan Rd, St Paul, MN 55126.

([parallel]) Sensotec, 2080 Arlingate Ln, Columbus, OH 43228.

(#) Heath Kit, 455 Riverview Dr, Benton Harbor, MI 49022.

(**) Autogenic Systems, 620 Wheat Ln, Wood Dale, IL 60191.

([dagger]) ([dagger]) Gould Inc, 3631 Perkins Ave, Cleveland, OH 44114.

([double dagger] [double dagger]) AR Vetter Co, Box 143, Rebersburg, PA 16872.

([subsections]) JVC Company of America, 41 Slater Dr, Elmwood Park, NJ 07407.

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BF Miller, ATC, is currently pursuing a PhD in integrative biology at the University of California-Berkeley, Berkeley, Calif. This work was performed in partial fulfillment of the degree requirements for Mr Miller's Master of Science degree in kinesiology at the University of Wisconsin-Madison.

KG Gruben, PhD, is Assistant Professor, Departments of Kinesiology and Biomedical Engineering, University of Wisconsin-Madison.

BJ Morgan, PT, PhD, is Associate Professor, Physical Therapy Program, Department of Surgery, University of Wisconsin-Madison. Address correspondence to Dr Morgan at 5173 Medical Sciences Center, 1300 University Ave, Madison, WI 53706-1532 (USA) ([e-mail]).

Writing and data analysis were provided by Miller, Gruben, and Morgan; concept and research design, by Miller and Morgan; facilities and equipment, by Gruben and Morgan; and data collection, project management, and subjects, by Miller. Dominic Puleo contributed to the data analysis and provided expert technical advice and support. Patricia L Mecum provided assistance with preparation of the manuscript, and Dr Peter Hanson provided consultation (including review of the manuscript before submission).

This study was approved by the Health Sciences Human Subjects Committee of the University of Wisconsin-Madison.

This article was submitted February 9, 1999, and was accepted August 23, 1999.