Pp
Original Research E. Ariel, BPT, MA Occ. Health, Sackler Faculty of Medicine, Tel Aviv University, POB 39040 Ramat Aviv, Tel Aviv 69978, Israel. Address all correspondence to Ms Ariel at: arielefr@tauex.tau.ac.il.
M. Ratmansky, MD, Sackler Faculty of Medicine, Tel Aviv University; and Pain Unit, Loewenstein Hospital Rehabilita- tion Center, Raanana, Israel.
Y. Levkovitz, MD, Sackler Faculty of Medicine, Tel Aviv University.
I. Goor-Aryeh, MD, Pain Clinic, Sheba Medical Center, Tel Hashomer, Ramat- Gan, Israel.
[Ariel E, Ratmansky M, Levkovitz Y, Goor-Aryeh I. Efficiency of tissue pen- etration by currents induced by 3 electrotherapeutic techniques: a com- parative study using a novel deep- tissue measuring technique. Phys Ther. 2019;99:540–548.]
C© 2019 American Physical Therapy As- sociation
Published Ahead of Print: January 17, 2019
Accepted: September 18, 2018 Submitted: February 1, 2018
Efficiency of Tissue Penetration by Currents Induced by 3 Electrotherapeutic Techniques: A Comparative Study Using a Novel Deep-Tissue Measuring Technique Efrat Ariel, Motti Ratmansky, Yechiel Levkovitz, Itay Goor-Aryeh
Background. Electrotherapy provides a wide range of treatment alternatives for mus- culoskeletal pathologies. However, for the electrical stimulation to exert a significant ther- apeutic effect, the induced current must often penetrate deep inside the target tissue.
Objective. The objective was to systematically compare the penetration efficiency of 3 electrotherapeutic stimulation modalities: transcutaneous electrical nerve stimulation (TENS), interferential (IF) stimulation, and combined therapy with pulsed ultrasound and IF current (CTPI).
Design. This was a comparative, experimental laboratory study.
Methods. The penetration efficiency was evaluated as a voltage difference between 2 of an 8-contact spinal cord stimulation array. Each of 20 participants with a preimplanted spinal cord stimulation array was stimulated with TENS (3 different electrode configura- tions), IF current (3 configurations), and CTPI (1 configuration).
Results. Significant differences in penetration efficiency were found between the various stimulation conditions and electrode configurations. CTPI showed the highest penetration efficiency, followed by IF, and finally TENS. Penetration efficiency was inversely and signif- icantly correlated with skinfold thickness in all conditions, but this correlation was lowest for the CTPI stimulation.
Limitations. Our study design did not include a condition of combined therapy with pulsed ultrasound and TENS, and it did not directly control for current or voltage density under the stimulating electrodes. In addition, further research is required to determine whether a higher stimulation intensity of the target tissue is advantageous clinically.
Conclusions. Pending further testing, CTPI stimulation could prove more effective than IF and TENS in reaching deeper tissues, especially considering the variability in adipose tissue thickness in the population, for example, in cases of patients with obesity.
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E lectrotherapy is an established componentof physical therapy1 and has shown numeroustherapeutic effects, including alleviating acute and chronic pain, healing tissues, reducing swelling, strengthening muscle tissue, and more.1–9 Although several electrotherapeutic techniques exist in the market, clinicians often need to rely on marketing information—rather than on scientific data—when choosing which technique to employ for a given indication. The reliance on marketing rather than data-driven evidence has been attributed to the absence of objective comparisons of the effects of specific stimulation parameters on specific clinical signs/symptoms.8,10,11 A major factor in the efficacy of electrotherapy is the degree to which the relevant tissue absorbs the applied energy11; because typical electrotherapy involves placing surface electrodes on the skin, the degree to which current from these electrodes penetrates into the tissue is of crucial importance. For instance, it has been shown that deeper penetration is a prerequisite for treating deep muscles,12,13
nerve-root irritation due to disk prolapse,14 and other pathologies.15 Two major factors have been notably implicated in controlling the depth of penetration of current applied through skin-surface electrodes: the type of current and the spatial configuration of electrode placement on the skin.16–22 Although some laboratory models have been reported,20,23 empirical and systematic studies of the effect of these factors on current penetration are relatively few, and they have mostly focused on the quadriceps muscle.16–19,24 This gap in knowledge appears to stem, at least in part, from methodological issues: namely, the current from the stimulating electrodes often causes muscle twitching, which disrupts electromyographic readings. This apparently inherent problem can be circumvented by inserting a recording electrode deep into the tissues, but the invasive nature of this technique has hindered patient recruitment, resulting in few empirical studies.20,23
In the current study, we employed a spinal cord stimulation (SCS) electrode array to characterize, as a proxy for current penetration efficiency, how voltage—applied through skin-surface stimulating electrodes and at various test conditions and electrode configurations—propagates through the tissue to reach the spinal cord. The SCS array was initially implanted in the mid-lower back of 20 participants as part of their pain management therapy. As test conditions, we employed the parameters often used in 3 common electrotherapeutic techniques1:
Transcutaneous electric nerve stimulation (TENS), in which low-frequency electrical pulses are conveyed through 2 skin-surface electrodes.
Interferential (IF) current stimulation, in which high-frequency, amplitude-modulated electrical bursts are conveyed through 2 pairs of skin-surface electrodes.
Notably, because of its high carrier frequency, IF stimulation had been postulated to penetrate to deeper tissues than TENS.22,25
Combined therapy with pulsed ultrasound and interferential current (CTPI), in which IF currents are applied simultaneously with ultrasound pulses. Although the CTPI mode is available in most contemporary electrical stimulation systems and has shown some clinical utility,2,26–28 its advantages vis-à-vis current penetration within deeper tissues of the mid-lower back region had not been tested.
Methods Participants The recruited participants were 20 adults (13 men; mean [SD] age = 61.0 [16.2] years; range = 28–80 years) (Table) who had different types of chronic pain—most commonly chronic low back pain and referred pain to 1 or both legs. As part of their chronic pain management at the pain clinic of the Sheba Medical Center, Tel Ha-Shomer (Ramat-Gan, Israel), these participants underwent a 1-week trial spinal cord stimulation (SCS) procedure, during which an electrode array with 8 contacts was implanted in their mid-lower back (see “Recording” below). Prior to implementing the SCS array, all participants were screened for typical electrotherapy contraindications according to the list provided by Watson.11 For inclusion in the current study, they were then screened again to exclude those with a history of traumatic brain injury and systemic diseases that might affect sensation. Prior to conducting the experiments, all participants were briefed verbally and in writing on the experimental procedure and signed an informed consent form. The study complied with the Declaration of Helsinki and was approved by the Human Ethics Committee of the Sheba Medical Center and of Tel Aviv University.
Study Design The study took place at the end of a 1-week SCS trial, conducted at the pain clinic of the Sheba Medical Center, during which participants were implanted with a temporary SCS electrode array prior to a permanent implantation. One day before the end of this trial and the removal of the temporary SCS array, the participants were contacted by phone, asked to participate in the study, and received a written explanation. Then, at the end of the SCS trial period and immediately before removal of the temporary SCS array in the pain clinic, the participants were briefed, signed an informed consent form, filled in a demographic questionnaire (including age, weight, height, number of years with chronic pain, physical condition, and physical exercise), and their skinfold thickness was measured 3 times from the lower thoracic area (20 cm lateral to the spinous process, at the T10-T11 level) with a FatTrack PRO digital caliper (AccuFitness, Denver, CO, USA). Finally, the participants were instructed to lie prone
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in a closed room, and brand-new adhesive stimulating electrodes were attached to the skin according to the planned electrode configurations (see “Stimulation” below).
During the experiment, the current applied through the stimulating electrodes was first increased in 2-mA increments until the sensation threshold of each participant was reached. Then, the current was further increased, using the same staircase method,29 until the patient indicated the onset of perceiving a painful stimulus, defined as the pain threshold. Throughout the experiment, the stimulating current was induced at 90% of the individual’s pain threshold. Each participant received all 7 types of test conditions (see below) sequentially (randomized between participants). Each of the 7 test procedures lasted between 3 and 7 minutes, and intertreatment duration was approximately 10 minutes.
Recording The trial SCS electrode array was implanted epidurally in the mid-lower back of each participant (positioned individually, according to the characteristic of the participants’ chronic pain; Table), at a depth of 3.5–6 cm from the skin (depending on the body mass index of the participant and determined using x-rays). The array (SCS Octrode model 3068 IFU; Medogar, Ra’anana, Israel) was 52 mm in length and comprised 8 linearly arranged platinum-iridium contacts (3-mm contact length; 4-mm intercontact spacing; contact resistance, <10 �; Figs. 1A and 1B), connected to a 60-cm, polyurethane-coated lead wire that protruded percutaneously outside the lower back of the participant. For the purpose of this study, we recorded the voltage difference between electrode 5 and electrode 2 (a ground reference on the oscilloscope) of the SCS array; we refer to this voltage, recorded deep within the tissue, as Vin. In addition, we recorded the voltage on the stimulating surface electrodes, which we refer to as Vout, by using crocodile clips connected to the surface of the pad (Fig. 1A).
Both the clips from the stimulating pad electrodes and the recording SCS electrodes were connected to a 2-channel, 100-MHz oscilloscope (model DPO2012b; Tektronix, Shanghai, China) to record Vout and Vin, respectively, at a sampling rate of 12.5 MHz. For the purposes of this study, penetration efficiency was defined as Vin/Vout, presented as a percentage.
Stimulation The stimulating electrodes (ValuTrode CF5090 with MultiStick conducting gel; Axelgaard, Fallbrook, CA, USA) were adhesive pads measuring 5 × 9 cm (for TENS and IF) and 7.5 × 13 cm (for CTPI) (Fig. 1). The electrodes were connected to a Sonopuls 491 stimulator (Enraf-Nonius, Rotterdam, the Netherlands), which is widely used in clinical practice. We used x-ray images of the participants to identify the location of each of the 8 contacts of the SCS
array and placed the stimulating electrodes on the skin at the same level as the recording contact (Fig. 1). To maintain consistency between all stimulation conditions (TENS, IF, and CTPI), we used the same stimulation frequencies (30 Hz) and pulse durations (250 μs; resulting in 125-μs phase durations) for all conditions—parameters that we had previously shown to be effective in reducing pain.29 For TENS and IF stimulation, we also tested the effect of various electrode configurations on the penetration efficiency of the applied currents. Thus, in addition to the most widely used TENS and IF electrode configurations—namely, placing the electrodes dorsally on both sides of the spinous process—we also tested the effect of placing the electrodes dorsoventrally (similar to the most widely used electrode configuration for CTPI) and/or along rather than on both sides of the spinous process. The electrode configurations are schematically shown in Figure 1 and are detailed below.
TENS condition. We applied biphasic symmetrical currents using 3 electrode configurations. In the TENS-1 configuration (Fig. 1D, top), which is the most commonly used TENS configuration,1 the 2 electrode pads were positioned dorsally on the paravertebral muscles, with 1 electrode on each side of the spinous process (1 cm lateral to the spinous process), such that the middle of each pad was placed at the level of the recording SCS contact. In the TENS-2 configuration (Fig. 1D, middle), the 2 electrode pads were positioned dorsally along the spinous process, such that 1 pad was placed 1 cm rostral, and the other 1 cm caudal, to the position of the recording SCS contact. In the TENS-3 configuration (Fig. 1D, bottom), a dorsal electrode pad was positioned over the spinous process (with the middle of the pad at the level of the recording SCS contact), and a ventral electrode pad was positioned at the same level on the abdomen. Stimulating intensities at 90% of the pain threshold for the TENS condition, reported as mean [SD] (range), were as follows (Table): TENS-1: 25.8 [15.0] (7.8–59) mA; TENS-2: 24.2 [13.2] (7.6–54.0) mA; and TENS-3: 24.6 [14.3] (7–61) mA.
IF condition. We applied amplitude-modulated sinusoidal currents with a 4-kHz carrier frequency using 3 electrode configurations. In the IF-1 configuration (Fig. 1E, top), which is the most commonly used IF configuration,1
the distance between each 2 adjacent electrode pads was 2 cm and the pads were positioned such that the recording SCS contact was directly between the 4 stimulating pads. In the IF-2 configuration (Fig. 1E, middle), 1 pair of electrode pads was positioned dorsally on the spinous process, and another pair of electrode pads was positioned at the same level on the abdomen. In each pair, the pads were placed 1 cm above and 1 cm below the recording SCS contact. In the IF-3 configuration (Fig. 1E, bottom), 1 pair of electrode pads was positioned dorsally on each side of the spinous process (1 cm from the spinous process) and the other pair was positioned at the same level on the abdomen. Stimulating intensities at 90%
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Figure 1. Study design. A, Example of stimulating electrode (SE) placement (TENS-2 configuration) on a participant. A spinal cord stimulating (SCS) electrode array (under the patch), which was preimplanted along the spinal cord of the participant, was used to record voltage by tapping into the extensions of the electrode contacts. B, Anterior-posterior x-ray of a patient, showing the position of the transplanted SCS electrode array and the percutaneous extending (Ext) lead wire. Voltage was recorded from contact 5 (SCS-5). C–E, Stimulating electrode configurations used in this study: C, combined therapy with pulsed ultrasound and IF current (CTPI); D, transcutaneous electrical nerve stimulation (TENS); and E, interferential (IF) stimulation. Green circle indicates the position of the recording SCS contact (not to scale). F, Sample recording (Vin, down-sampled to 2.5 kHz) from a typical participant, stimulated with an IF current.
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of the pain threshold for the IF condition, reported as mean [SD] (range), were as follows (Table): IF-1: 29.7 [13.1] (14.4–62) mA; IF-2: 27.8 [14.3] (9.0–58.0) mA; IF-3: 27.0 [16.0] (7–63) mA.
CTPI condition. An electrode pad was placed on the abdomen at the level of the recording SCS contact, and the ultrasound treatment head (5 cm2), coated with an ultrasound coupling gel (Intelect Ultrasound Gel; Chattanooga Medical Supply Inc, Chattanooga, TN, USA), was placed at the same level on the spinous process (Fig. 1C) and remained stationary throughout the measurements. The ultrasonic waves were delivered at 1.2 W/cm2 on a 20% duty cycle with a frequency of 1 MHz. The current delivered through the treatment head was a premodulated IF current with a carrier frequency of 4 kHz. The mean stimulating intensity for the CTPI condition was 24.0 (SD = 12.4; range = 7.0–45.0) mA.
Pilot Study In a pilot study, we determined how various factors affected the response of the SCS electrodes array in a controlled environment (tap water and saline) to stimulation at all 3 conditions. Briefly, this pilot study showed that: (1) the relationship between Vin and Vout was linear in all test conditions (TENS, IF, and CTPI currents; water and saline); (2) the distance between the stimulating and recording electrodes considerably affected Vin, such that, for a given Vout, Vin considerably increased as the distance between the stimulating and recording electrodes decreased; and (3) as long as the distance between the stimulating and recording electrodes remained constant, the depth to which the 2 sets of electrodes were immersed in tap water or saline did not significantly affect Vin. This finding indirectly suggests that Vout mainly affects Vin through the contacts, rather than through the lead wire.
Data Analyses Because of a relatively low sample size and a nonnormal distribution of the data, an aparametric test (related-samples Friedman 2-factor analysis of variance by rank) with Bonferroni correction was used to compare the penetration efficiencies (Vin/Vout, presented as a percentage) of the different test conditions. Correlations between penetration efficiency and skin-fold thickness were calculated by using the Spearman correlation coefficient. The significance level was set to .05 in all tests, and all data are presented as mean [SD]. All analyses were conducted with SPSS version 23 (IBM SPSS, Chicago, IL, USA).
Results Selected participant characteristics and the raw stimulating (Vout) and recorded (Vin) voltages for all participants are shown in the Table. Of all examined test conditions, CTPI showed the highest average penetration efficiency, followed by IF and, finally, TENS (Fig. 2). A summed comparison (using all electrode configurations of the same
condition lumped together) revealed that the average penetration efficiency of CTPI (26.71 [12.74]%) was significantly higher than that of TENS (10.28 [6.82]%, P ≤ .001) and IF (17.81 [9.04]%, P = .034), and that the penetration efficiency of IF was higher than that of TENS (P = .002). Pairwise comparisons within the TENS and IF conditions revealed that penetration efficiency was significantly greater for configuration TENS-3 than for configuration TENS-2 (P = .002), and for configuration IF-2 than for configuration IF-1 (P ≤ .001); all other within-group comparisons were nonsignificant (Fig. 2).
Spearman correlations (Fig. 3) showed that the penetration efficiency was inversely and significantly correlated with skin-fold thickness in all treatments (TENS: ρ = −0.777, P ≤ .001; IF: ρ = −0.689, P ≤ .001; CTPI: ρ = −0.46, P = .04). Importantly, of all 3 treatments, CTPI demonstrated the lowest correlation with skinfold thickness, although the difference in the correlation coefficients of the 3 conditions did not reach statistical significance.
Discussion We employed a novel measuring technique to characterize the penetration efficiency of currents induced by 3 common electrotherapeutic approaches: TENS, IF, and CTPI. Our results indicate that the CTPI condition provided the most efficient penetration, followed by IF and, finally, TENS. In addition, we found that the highest voltages recorded near the spinal cord were for dorsoventral (rather than dorsal) configurations, probably because the current passes directly through the recording site. Thus, despite the greater interelectrode distance in dorsoventral configurations (which is usually negatively correlated with penetration efficiency when large electrodes are used21), such configurations could be preferable over dorsal configurations when a greater current penetration depth is required. Notably, for similar interelectrode distances and electrode positions, IF stimulation appears to penetrate more effectively into the tissue than TENS (Fig. 2). Additionally, we found that penetration efficiency was inversely correlated with skin-fold thickness in all 3 test conditions, but this correlation was lowest for the CTPI treatment—further suggesting that CTPI could be the most effective approach for reaching deeper tissues, regardless of tissue composition. To the best of our knowledge, this is the first study to describe the penetration efficiency of CTPI treatment and systematically compare it with that of TENS and IF treatments. Our finding that CTPI can reach deeper tissues should encourage future studies to investigate both the underlying mechanisms and the optimal CTPI stimulation parameters for clinical applications.
The primary factors that affect density distribution of electrotherapeutic currents and their transmission into and within tissues likely involve the characteristics of the
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Tissue Penetration of Electrotherapeutic Currents
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Figure 2. Penetration efficiency (internal [recorded] voltage/external [stimu- lating] voltage, presented as percentage) according to treatment and electrode configurations. The box plots indicate the median (horizontal line), first and third quartiles (bottom and top box boundaries, respectively), and fifth and 95th percentiles (bottom and top whiskers, respectively). Empty circles represent outliers. ∗P < .05, ∗∗P < .01, ∗∗∗P < .001 (2-sided Friedman aparametric test with Bonferroni correction for between-group comparisons, and pairwise comparisons within each group). CTPI = combined therapy with pulsed ultrasound and interferential current; IF = interferential stimulation; TENS = transcutaneous electrical nerve stimulation.
stimulating current, the stimulated tissues, and, most importantly, the interaction between the two.19,20,30,31
Several studies have empirically characterized the penetration efficiency of TENS and IF stimulation (see, eg, refs 16,18,19), but the results of these studies vary quantitatively and qualitatively, both from each other and, in some parameters, from our results—probably due to methodological discrepancies (eg, electrical stimulation parameters, the position of the recording and stimulating electrodes, or the methods of recording voltage within the tissue).22,24 For instance, Petrofsky and colleagues used needle electrodes to measure the voltage penetrating into the quadriceps18,19 and found lower penetration efficiencies than those reported here, which can plausibly be explained by different electrode sizes and interelectrode distances. Indeed, such methodological differences highlight some of the inherent problems in adequately comparing the results across different studies, and the importance of comparing various stimulation parameters and electrode configurations in the same study, using a more controlled methodological approach. One important factor that we addressed here and that clearly influences the transfer of current to deeper tissues is the thickness of the adipose tissue.20,32 This factor appears to bear high clinical importance, because it varies considerably between individuals; for instance, in our 20-participant sample, skinfold thickness ranged between 9 and 23 mm, and it was significantly correlated with penetration efficiency in all 3 stimulation modalities.
Figure 3. Spearman correlations between skinfold and penetration efficiency in transcutaneous electrical nerve stimulation (TENS: top), interfer- ential (IF) stimulation (middle), and combined therapy with pulsed ultrasound and IF current (CTPI: bottom).
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Our study had limitations, mostly due to the methodological difficulty in studying the penetration efficiency of current in a clinical setting. First, we focused on the stimulation modes that are most commonly available in contemporary electrical stimulation systems, such that our study design did not include a combination of TENS with ultrasound (wherein the reference electrode is placed over the abdominals, like in the CTPI condition). Therefore, our conclusion that CTPI is preferred over TENS in reaching deeper tissues needs to be further validated, because combining TENS and ultrasound might yield an equal or even greater penetration efficiency than that of CTPI. Second, we did not directly control for current or voltage density under the stimulating electrodes, which might change between stimulation conditions33 and affect Vin. Third, to decrease the possible influence on our findings of potential habituation or facilitation of the pain thresholds within a single session, we randomized test conditions between patients and used the ratio Vin/Vout (rather than Vin alone) as a proxy for current penetration efficiency; however, we did not control for such effects directly. Finally, although higher stimulation intensity generally appears to have the strongest evidence of clinical efficacy,34 further systematic studies and randomized control trials are needed. For clinical applications, understanding penetration efficiency is just a step in developing guidelines for optimal treatment parameters for various clinical goals.
Conclusions We employed an implanted SCS electrode array to approximate the penetration efficiency of currents induced on the surface of the skin by TENS or IF stimulation (either alone or with ultrasound, namely, CTPI). Of the 3 modalities, CTPI stimulation demonstrated the most efficient current penetration, followed by IF stimulation and, finally, TENS. The penetration efficiency was significantly correlated with skinfold thickness in all experimental conditions, highlighting the influence of adipose tissue thickness on current penetration. Notably, because of an unidentified mechanism, this correlation was lowest for CTPI, which could have clinical implications when pain is perceived in deeper structures. Further studies are required to examine the current penetration efficiency in other stimulation modes and electrode configurations. Researchers are encouraged to employ more direct and objective measures of current intensity (eg, current density under the electrode), as well as to test the relationship between stimulation intensity of the target tissue and clinical outcomes.
Author Contributions and Acknowledgments
Concept/idea/research design: E. Ariel, M. Ratmansky, Y. Levkovitz, I. Goor-Aryeh
Writing: E. Ariel Data collection: E. Ariel
Data analysis: E. Ariel Project management: E. Ariel, Y. Levkovitz, I. Goor-Aryeh Providing participants: M. Ratmansky, I. Goor-Aryeh Providing facilities/equipment: E. Ariel, I. Goor-Aryeh Providing institutional liaisons: Y. Levkovitz Consultation (including review of manuscript before submitting):
M. Ratmansky, Y. Levkovitz, I. Goor-Aryeh
This work was conducted as part of a PhD thesis by EA, submitted to Tel Aviv University. We thank Dr Ram Gal and 2 anonymous reviewers for their helpful comments on the manuscript.
Ethics Approval
The study complied with the Declaration of Helsinki and was approved by the Human Ethics Committee of the Sheba Medical Center and of Tel Aviv University.
Funding
There are no funders to report for this study.
Disclosures
The authors completed the ICJME Form for Disclosure of Potential Conflicts of Interest and reported no conflicts of interest.
DOI: 10.1093/ptj/pzz005
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