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Research Reports |
ML Sandberg, PT, PhD, is Researcher and Lecturer, Department of Rehabilitation Medicine, Faculty of Health Sciences, and Pain and Rehabilitation Centre, University Hospital, S-581 85 Linköping, Sweden
MK Sandberg and J Dahl were students in the Physiotherapy Program, Faculty of Health Sciences, Linköping University, Linköping, Sweden, at the time of this study
Address all correspondence to Dr Sandberg at: margareta.sandberg{at}lio.se
Submitted June 21, 2006;
Accepted March 15, 2007
 | Abstract |
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Subjects: Thirty-three women who were healthy, aged 25 to 55 years, were randomly assigned to receive 1 of 3 different modes of TENS.
Methods: Skin and muscle blood flow were monitored noninvasively using a new application of photoplethysmography for 15 minutes of TENS applied at high frequency (80 Hz) and sensory-level intensity and at low frequency (2 Hz) and motor-level intensity and for 15 minutes after stimulation. Subliminal 80-Hz TENS was used as a control. Blood flow was monitored simultaneously on stimulated and nonstimulated shoulders.
Results: Blood flow in the trapezius muscle, but not skin blood flow, increased significantly with motor-level 2-Hz TENS, whereas no increase occurred with sensory-level 80-Hz TENS or subliminal 80-Hz TENS.
Discussion and Conclusion: Muscle contractions induced by motor-level 2-Hz TENS appear to be a prerequisite for increasing blood flow in the trapezius muscle. However, high stimulation intensity may prevent increased blood flow in the overlying skin.
| Introduction |
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 TopAbstract Introduction MethodResultsDiscussionConclusionReferences |
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In a study by Wikström et al,3 skin blood flow in participants who were healthy was increased with TENS of low frequency (2 Hz) but not with TENS of high frequency (100 Hz), whereas in another study,4 skin blood flow in ischemic tissue was found to increase with TENS of 80 Hz, eliciting a strong tingling sensation. Low-frequency TENS (2 Hz) of the highest tolerable intensity, but not by low-intensity stimulation, increased microcirculation in patients with chronic leg ulcers.5 However, in the tissue surrounding the ulcers, the blood flow increase was substantially less. Moreover, low-frequency TENS (4 Hz), but not high-frequency TENS (110 Hz), applied over the median nerve in subjects who were healthy resulted in increased skin blood flow, provided that the stimulation intensity was above the motor threshold level.6,7 The different results of these studies probably reflect differences in stimulation parameters and in stimulation and recording sites, the circulatory status of the tissue, and different properties of the measuring techniques. Studies of TENS frequently use laser Doppler flowmetry (LDF)8 and venous occlusion plethysmography9 to measure blood flow changes in skin and volume changes in a limb segment, respectively.
The effect of TENS on local muscle blood flow has not been investigated previously. This may be the case because an appropriate measurement technique has not been available. Although further developments of the LDF technique allow blood perfusion to be measured invasively in local muscle tissue,10 one drawback of the method is the trauma caused by the insertion of the optic fiber, which affects the blood flow. Thus, the invasive LDF technique is not a suitable technique when investigating local effects of TENS on muscle blood flow. Changes in muscle blood flow may be estimated indirectly by measuring total blood flow in a limb segment using techniques such as venous occlusion plethysmography.9 Using this technique, burst-mode TENS (burst frequency of 20 and 2 Hz, respectively) with an intensity high enough to cause muscle contractions has been shown to increase calf blood flow.11,12
Photoplethysmography (PPG) is an established optical technique for continuous skin blood flow monitoring.13,14 In PPG, light from a light-emitting diode (LED) is directed toward the skin and is absorbed and scattered in the tissue. A small amount of this light is received by a photodetector placed adjacent to the LED (reflection mode). Variations in the photodetector signal are related to changes in blood flow and blood volume in the underlying tissue. With the use of custom-designed optical probes with accompanying PPG instrumentation, PPG recently has been used for noninvasive continuous measurements of blood flow changes in the tibialis muscle15,16 and the trapezius muscle17 following needle stimulation (acupuncture). Noninvasive measuring methods have large advantages over invasive methods because they do not interfere with the local blood flows under study.
The purpose of the present study was to investigate the effects of TENS on blood flow in the trapezius muscle and overlying skin in women who were healthy using a new noninvasive application of PPG. Because our main interest was directed toward effects on muscle blood flow, we chose to use TENS of high intensity, but below the limit of discomfort, as determined individually by the subjects. We also chose to use TENS of both low and high frequency, although our hypothesis was that low-frequency TENS would be the most effective mode.
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TopAbstractIntroductionMethodResultsDiscussionConclusionReferences |
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Blood Flow Recording
A new application of PPG (currently under development and not yet commercially available1,*) was used in the present study to monitor blood flow changes simultaneously in the trapezius muscle and overlying skin. The custom-designed PPG probes (48 x 40 mm) for the trapezius muscle consisted of 4 photodetectors, 4 green (560-nm) LEDs, and 2 near-infrared (804-nm) LEDs placed in a special pattern and embedded in black-colored silicon (Fig. 1). The center-to-center distance between the LEDs and the photodetectors was 3.5 mm and 25 mm for wavelengths of 560 and 804 nm, respectively. The 560-nm LED monitored the superficial blood flow, and the 804-nm LED monitored the deeper blood flow (preferentially the muscle flow). The LED at 804 nm ensures that the blood flow signal will not be affected by variations in oxygen saturation.
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Transcutaneous Electrical Stimulation
A pocket-sized, 2-channel stimulator (CEFAR Primo model2,
) was used for the electrical stimulation. The TENS unit delivered constant asymmetrical biphasic balanced square-wave pulses of high frequency (80 Hz) and low frequency (2-Hz burst mode, 8 pulses per burst) with a pulse duration of 180 microseconds. Motor-level 2-Hz TENS was intended to elicit strong, but not painful or unpleasant, contractions of the shoulder muscles, and sensory level 80-Hz TENS was intended to elicit strong sensations of paresthesia, but not muscle contractions. Subliminal 80-Hz TENS with the lowest possible current intensity (0.5 mA), resulting in no sensation at all, was used as a control. Two 40- x 60-mm electrodes were used.
Procedure
The subjects were randomly assigned, in equal numbers, to one of the three 15-minute TENS interventions (sensory-level 80-Hz TENS, motor-level 2-Hz TENS, or subliminal TENS) by the use of opaque sealed envelopes. The trial was conducted in a quiet room with moderate light and a temperature between 23° and 25°C. The subjects sat with bare upper body in an armchair with their back supported up to the lower part of the scapulae and with their arms resting on a cushion on their knees. They were instructed to sit relaxed and not to talk during the blood flow recordings. The PPG probes were attached with adhesive tape to the most prominent part of the trapezius muscles of the right and left shoulders. If necessary, the probes were moved slightly in order to detect signals. Two electrodes then were attached to the skin on either side of the PPG probe on the dominant shoulder. With the motor-level 2-Hz TENS, the cathode was placed over the medial part of the trapezius muscle. With the sensory-level 80-Hz TENS and subliminal TENS, the cathode was placed over the lateral part of the muscle.
Sensory and motor thresholds were noted for each subject. The sensory threshold was determined and quantified by the current intensity (in milliamperes) that elicited the first sensation of the stimulation. The motor threshold was determined and quantified by the current intensity of motor-level 2-Hz TENS that elicited the first sensation of contraction of the muscle. The subjects were informed that the stimulation during the trial would elicit a strong, but not painful, sensation of paresthesia with sensory-level 80-Hz TENS, visible muscle contractions with motor-level 2-Hz TENS, and no sensation with subliminal TENS. They also were informed that the stimulation intensity would be increased, if necessary, in order to maintain the initial sensation.
The investigation started after at least 20 minutes of acclimatization. The different types of TENS interventions lasted 15 minutes. The current intensity with sensory- and motor-level TENS was increased quickly until the subject felt minor discomfort and then was immediately decreased below this limit, as determined individually by the subjects. Immediately after the trial, the subjects rated the pain or discomfort that they experienced during the trial using a visual analog scale (VAS).
Blood flow was recorded for 60 seconds before the intervention and then intermittently for 60 seconds every 3 minutes during the 15-minute stimulation and for another 15 minutes after stimulation. During the last 20 seconds of the recordings during stimulation, the current was abruptly switched off to allow for clear PPG signals for analyses and then quickly switched on again. The signals were processed in an amplifier and stored on a personal computer.
Data Analysis
Blood flow changes, based on the last 20 seconds of the 60-second recordings, were expressed as a percentage of the resting (baseline) value (denoted as 0). Mean values of stimulation and poststimulation periods were calculated and used for nonparametric analyses using the Statview 5.1 statistical package.
The Kruskal-Wallis test was used to test for differences between groups. The Mann-Whitney U test was used for pair-wise comparisons of significant findings. The Wilcoxon matched-pairs signed-ranks test was applied for pair-wise comparisons within groups and to test for differences between the stimulated and nonstimulated shoulders. A P value of <.05 (two-tailed) was considered significant. Figures 2 and 3 show the means and standard errors of the mean.
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| Results |
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TopAbstractIntroductionMethodResultsDiscussionConclusionReferences |
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A significant difference existed among the TENS interventions (P<.0001) in that the mean muscle blood flow increase was significantly larger with motor-level 2-Hz TENS compared with both sensory-level 80-Hz TENS (P=.001) and subliminal TENS (P=.001). No difference was found between sensory-level 80-Hz TENS and subliminal TENS. During the 15-minute post-stimulation period, no significant difference in mean blood flow increase was found between motor-level 2-Hz TENS and subliminal TENS, both of which were superior to sensory-level 80-Hz TENS (P=.004 and P=.034, respectively). Blood flow increase was significantly greater with motor-level 2-Hz TENS than with subliminal TENS until 3 minutes post-stimulation (P=.028).
To control for a potential warming effect of the measuring device on blood flow, simultaneous measurements were performed on the nonstimulated shoulder. No differences in mean blood flow increase existed among the TENS interventions in the nonstimulated shoulder, either during the 15-minute stimulation period or the 15-minute post-stimulation period (Fig. 3A). Only with motor-level 2-Hz TENS did a significantly larger mean blood flow increase exist in the stimulated shoulder than in the nonstimulated shoulder both during stimulation (P=.008) and after cessation of stimulation (P=.013). Significant increases in muscle blood flow during and after stimulation compared with baseline existed in the nonstimulated shoulder only with subliminal TENS (P=.011 and P=.008, respectively); however, these changes were not significantly different from those in the stimulated shoulder (Fig. 3A).
Skin Blood Flow
Relative changes in skin blood flow for the 3 TENS groups throughout the study period are shown in Figure 2B. No significant differences existed among the TENS interventions during or after cessation of TENS in either the stimulated shoulder or the nonstimulated shoulder (Fig. 3B). Only with subliminal TENS was an increase found in mean blood flow during stimulation (P=.008); however, this increase was not significantly different from the increase in the nonstimulated shoulder (Fig. 3B). During the post-stimulation period, an increase existed in mean blood flow with motor-level 2-Hz TENS (P=.028) and subliminal TENS (P=.011); however, this increase was not significantly different from that in the nonstimulated shoulder (Fig. 3B).
| Discussion |
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TopAbstractIntroductionMethodResultsDiscussionConclusionReferences |
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Methodological Considerations
Different electrical stimulation parameters between and within groups were used in the study. First, the placement of cathode and anode was reversed with motor-level 2-Hz TENS and sensory-level 80-Hz TENS. In order to facilitate muscle contractions with motor-level 2-Hz TENS, the cathode was placed over the most prominent part of the muscle belly, medial to the PPG probe. With sensory-level 80-Hz TENS, the cathode was placed lateral to the probe to minimize the risk of producing muscle contractions. Second, 2 different frequencies were used: 2 Hz (motor-level TENS) and 80 Hz (sensory-level TENS). Motor-level 2-Hz TENS was intended to produce visible muscle contractions, and sensory-level 80-Hz TENS was used to elicit a strong, but not painful, sensation of paresthesia.
Third, the intensity of stimulation differed between the groups, with motor-level 2-Hz TENS having a higher intensity and sensory-level 80-Hz TENS having a lower stimulation intensity. Fourth, the intensity of the stimulation was not fixed, but differed among the subjects during the 15-minute stimulation period. In order to produce continuously strong, but not painful, muscle contractions and paresthesia, respectively, throughout the 15-minute TENS intervention, a fixed stimulation intensity could not be used, but had to be individually adjusted. Thus, the rationale for using different electrical stimulation parameters was based on the purpose of each type of stimulation (ie, to produce and maintain a similar level of muscle contractions and paresthesia, respectively).
To our knowledge, noninvasive real-time measurement of local muscle blood flow following TENS has not been performed previously. Venous occlusion plethysmography9 has been used to examine hemodynamic effects of TENS; however, this examination showed only increased calf blood flow following electrical stimulation above the motor threshold.11,12 This technique is based on determining total volume increase versus time in an entire limb segment when venous outflow is arrested and does not allow skin and muscle blood flow to be measured separately. Because different measurement techniques have been used in studies on hemodynamic effects of TENS, results are not fully comparable. Furthermore, different measurement techniques rely on different technical principles and measure different vascular beds.
One drawback of the PPG probe in long-term monitoring is a warming effect from the light sources, leading to a local temperature increase and local blood flow regulation.18 It has been shown that the warming effect from the probe during long-term monitoring induces an increase of up to 20% in the trapezius muscle blood flow and overlying skin.18 This level of blood flow increase corresponds approximately to the muscle blood flow increase with subliminal TENS in the present study, thus rendering subliminal TENS a suitable and valid control in this respect.
As for skin blood flow, the use of subliminal TENS as a control might be uncertain because skin blood flow increase following cessation of stimulation was slightly more than the 20% mentioned above.18 However, the increase in blood flow with subliminal TENS was not significantly different from the skin blood flow increase in the contralateral, nonstimulated shoulder. In addition, it was not until the end of the stimulation period that the increase was apparent. It also should be emphasized that the TENS electrodes themselves may inhibit convection, thereby giving rise to increased skin temperature and a subsequent rise in skin blood flow due to temperature regulation effects in the stimulated shoulder.19
A possible limitation of the study may be the relative short stimulation time of 15 minutes; however, this period of stimulation also has been chosen in other studies.6,7 An apparent limitation was that the PPG technique did not permit measurements during the dynamic muscle contractions. This limitation is similar to that of other measurement techniques, such as Doppler flowmetry. Thus, in the present study, TENS was interrupted for 20 seconds every 3 minutes for measurements. This means that the effect of motor-level 2-Hz TENS, which turned out to be the mode of stimulation of interest, could be assessed only as immediate post-exercise hyperemia, not as a result of ongoing contractions induced by TENS.
The subjects were told that the stimulation would be strong, but not uncomfortable or painful. During the stimulation, the subjects were repeatedly asked to report whether the intensity decreased; if this was the case, the intensity was increased again in order to maintain the initial sensation. This procedure may have encouraged the subjects to accept an intensity that was more intense than intended because, after the end of the study, some of the participants reported either slight discomfort or pain from the stimulation.
One benefit of the study was the use of bilateral measurements. Because a warming effect of the PPG probe is known from previous studies,15–18 blood flow measurements were performed bilaterally, although the electrical stimulation was applied only unilaterally. Few studies use bilateral measurements to control for effects on blood flow induced by the measurement device itself.
Muscle Blood Flow Changes
Post-exercise hyperemia is a well-known phenomenon after both static and dynamic contractions.20 It is generally believed that exercise hyperemia is a local phenomenon including myogenic, metabolic, and endothelium-mediated control.21 The "muscle pump" accumulation of local metabolic vasodilator substances and flow-induced vasodilation produced by local release of relaxing factors derived from the endothelium were suggested as potential mechanisms for the observed vasodilation in the study by Sherry et al12 following burst-mode TENS 25% above motor threshold.
Although muscle blood flow increased significantly with subliminal TENS, this effect was not caused by the stimulation itself but rather was induced by the warming effect of the PPG probe.17 This conclusion can readily be drawn by the finding of an equal level of blood flow increase in the contralateral trapezius muscle. In addition, blood flow with subliminal TENS tended to increase not until the end of stimulation, further pointing to a temperature regulation effect (Figs. 2B and 3B). A corresponding warming effect on blood flow was not observed with sensory-level 80-Hz TENS. Some subjects reported unpleasantness or slight pain from the stimulation, and possibly the warming effect was overridden by increased sympathetic tone and vasoconstriction as a result of the high stimulation intensity.
Using occlusion plethysmography, a transient and similar level of increase in calf blood flow following both voluntary contractions and burst-mode TENS (20 and 2 Hz, respectively) was observed when the intensity was 125% of the motor threshold.11,12 Similar to the present study, blood flow returned quickly to the baseline after cessation of stimulation. However, Miller et al11 showed that the electrically induced muscle contractions produced a vasodilatation of a slightly longer duration compared with the voluntary contractions. In another study,22 the effects on limb blood flow in subjects who were healthy with 110-Hz TENS applied for 20 minutes over the peripheral nerves were investigated using venous occlusion plethysmography. The results showed that neither sensory- nor motor-level TENS influenced calf blood flow. Although these studies used other parameters than in the present study, a trend toward the same conclusion seems reasonable: motor-level TENS eliciting strong rhythmic muscle contraction, but not sensory-level TENS, enhances circulatory effects of human muscle.
Compared with the present results on muscle blood flow, those induced by needle stimulation (acupuncture) in previous studies15,17 were of considerably longer duration. This finding may reflect different underlying mechanisms on blood flow induced by TENS and acupuncture.
Skin Blood Flow Changes
Studies on blood flow changes following TENS have dealt almost exclusively with skin blood flow measured mostly by LDF.8 Inconsistent results have been found depending on different parameters of stimulation (eg, intensity, frequency, site and duration of stimulation) as well as differences in recording sites and recording methods. Although both LDF and PPG are used to measure skin blood flow, results are not comparable because these modalities monitor different depths of vascular beds: LDF 
–1 mm and PPG 1–2 mm.18 Several authors3,5–7,23 have reported an increase of skin blood flow following low-frequency TENS. Cramp et al6 found that 15 minutes of low-frequency TENS (4 Hz) resulted in significantly larger increases in local skin blood flow compared with high-frequency TENS (110 Hz) using "strong but comfortable sensation" or TENS electrodes only (control) over the median nerve. They found that skin blood flow quickly and significantly increased during the application of 4-Hz TENS, followed by a rapid and distinct drop after cessation of stimulation, although skin blood flow remained significantly above the baseline level by 30% for 15 minutes post-stimulation.
This pattern of response was quite different from that found in the present study, where a continuous, although nonsignificant, increase was seen even after the cessation of stimulation. The different results may have various explanations, such as differences in stimulation intensities and stimulation sites. In the present study, motor-level 2-Hz TENS, causing visible muscle contractions, may have resulted in redistribution of blood from the skin to the contracting trapezius muscle underneath.19 The finding in the present study that increases in skin blood flow with motor-level 2-Hz TENS were not significantly different from increases in skin blood flow in the contralateral, nonstimulated shoulder suggests that this mode of stimulation may not result in true increases in skin blood flow.
With 15-minute sensory-level TENS, skin blood flow did not increase in either the present study using a frequency of 80 Hz or in the study by Cramp et al,6 who used a frequency of 110 Hz at an amplitude causing a "strong but comfortable sensation." A blood flow increase of 15% to 20% should be expected due to the warming effect of the PPG probe. Consequently, a decrease rather than an increase in skin blood flow might have been the result of the stimulation, possibly reflecting increased sympathetic activity causing cutaneous vasoconstriction and decreased skin blood flow. This increased sympathetic activity may be explained by the high stimulation intensity, which at times was perceived as unpleasant or painful. In contrast to these studies, however, a study comprising assessment after repeated 2-hour sessions per day (sensory-level 80-Hz TENS) in ischemic tissue showed increased skin blood flow.4
In the present study, subliminal TENS with the weakest current intensity possible (0.5 mA) was chosen as a control and was not expected to affect blood flow. This intensity corresponded to no more than 0.2 times the sensory threshold. Although skin blood flow did increase with this stimulation, it was not significantly different from the increase in skin blood flow in the contralateral, nonstimulated shoulder. It is possible that the TENS electrodes might have induced a warming effect, affecting skin blood flow. Cramp et al6 found no increase in skin blood flow for their nonactivated TENS electrodes on the medial side of the forearm. However, these studies used disparate stimulation and recording sites, which make comparisons of results difficult.
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| Footnotes |
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The local ethics committee at the Faculty of Health Sciences, Linköping University, approved the study.
This study was supported by grants from the County Council in Östergötland, Sweden.
* Department of Biomedical Engineering, Linköping University, S-581 85 Linköping, Sweden. 
CEFAR Medical AB, Ideon SciencePark, Scheelevägen 19A, SE-223 70 Lund, Sweden.
SAS Institute Inc, PO Box 8000, Cary, NC 27511.
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