Therapeutic ultrasound is one of the most commonly used modalities in physical medicine and rehabilitation. Adding therapeutic ultrasound before range of motion techniques to treat joint contractures has resulted in positive clinical outcomes.1–3 Therapeutic ultrasound in combination with stretching created acute range of motion increases over stretching alone.4 In patients with decreased wrist flexion and/ or extension, heating the tissue with therapeutic ultrasound before joint mobilizations restored normal range of motion within six treatment sessions.1,3
Therapeutic ultrasound produces mechanical and thermal physiological effects. The mechanical effects of stable cavitation and microstreaming have been determined through in vitro thermal neutral environments. From these studies, it has been hypothesized that mechanical efforts aid in the tissue healing process through ion transport, promoting cellular permeability, and altering enzyme function.5 Temperature-based treatment goals are often used to determine the thermal physiological effects.6 It has been suggested that mild heating (Δ 1°C) increases tissue metabolic rate and moderate heating (Δ 2°C to 3°C) causes muscle spasm relaxation, modulates pain, and increases blood flow. Vigorous heating (Δ ≥ 4°C or tissue temperature increase to Δ 40°C) has been suggested to alter the viscoelastic properties of collagen.7–9
Based on therapeutic ultrasound's thermal effects and temperature-based goals, clinicians should apply range of motion techniques when tissues are at the suggested intramuscular temperature. The “stretching window” has been defined as “the time during which the tissue temperature is ideal to apply stretching and joint mobilization procedures to efficiently increase collagen extensibility.”10 The stretching window occurs while the tissue temperatures are greater than 3°C from baseline temperatures.11 For example, a previous calculation of the stretch window after a 3-MHz therapeutic ultrasound treatment with an intensity of 1.5 W/cm2 indicates clinicians should apply range of motion techniques within 3.3 minutes of the cessation of the treatment.11
The stretching window has been determined for 3- and 1-MHz therapeutic ultrasound frequencies but only using one intensity (1.5 W/cm2).10,11 Different therapeutic modalities have different heating capacities and heating rates, leading to different temperature decays.12,13 It is unknown whether different therapeutic ultrasound intensities, creating different heating rates, would also alter the temperature decay characteristics and change the stretching window time. The purpose of our study was to determine whether two different therapeutic ultrasound intensities would increase tissue temperature by 5°C in different times and whether the different heating rates would alter the length of the stretching window.
We used a cross-over controlled design to determine tissue temperature rise and decay at different ultrasound intensities. The dependent variables were: (1) treatment time to reach a 5°C increase in intramuscular temperature, (2) time for intramuscular temperature to decay 2°C or more, (3) time for intramuscular temperature to decay 3°C or more, and (4) time for intramuscular temperature to return to baseline. Intramuscular temperature was measured at a 1.2 cm depth in the triceps surae muscle group every 30 seconds throughout the treatment and after treatment (ie, temperature decay). The independent variable was ultrasound intensity with two levels: high = 1.7 W/cm2 and low = 1.0 W/cm2. Ultrasound intensities were selected based on their ability to heat intramuscular muscle at different rates but still reach the desired tissue temperature threshold.7 All treatments were administered using a 3-MHz frequency. This study was designed to match previous stretching window study procedures, specifically related to the procedures associated with tissue temperature increase threshold (Δ 5°C) and insertion depth of the temperature probe (1.2 cm).11
Eighteen participants (9 men and 9 women, age = 25.2 ± 2.6 years, height = 173.4 ± 12.7 cm, mass = 81.4 ± 20.0 kg) were enrolled in the study. We randomized the participants into a counter-balanced treatment order. Participants were included in the study if they were healthy individuals and were excluded based on the following criteria and contraindications for therapeutic ultrasound: fever, infection, or lesions in the lower leg, compromised circulation or sensation within the lower leg, or injury to the triceps surae muscle group within the past 2 months. Participants were not allowed to take pain medications prior to or during the study because some pain medications (eg, commonly used nonsteroidal anti-inflammatory drugs) may cause thinning of the blood. This thinning of the blood may affect local tissue heating and cooling rates. All of the participants were informed of the possible risks related to this study and signed an institutional review board–approved consent form. Before enrolling participants, this study was reviewed and approved by the institutional review board at Weber State University.
All treatments were administered with a recently calibrated Omnisound 3000 (Accelerated Care Plus, Reno, NV) with a 5 cm2 transducer. The effective radiating area and beam non-uniformity ratio of the transducer specific to 3 MHz were 5 cm2 and 1.9:1, respectively.
Intramuscular tissue temperature was measured using a 23-gauge needle temperature probe (MT 23/5; Physitemp Instruments, Inc., Clifton, NJ), which interfaced with a recently calibrated Iso-thermex electrothermometer (Isothermex 256; Columbus Instruments, Columbus, OH). The Isothermex electrothermometer has previously been found to be reliable (±0.03°C) between measurement sessions and valid within 0.06°C of a mercury NIST calibrated thermometer.14 All temperature probes were cleansed (Enzol; Johnson & Johnson, New Brunswick, NJ), sterilized with a sterilizing solution (Metricide 28; Metrex Research, Orange, CA), and rinsed with sterile water before use.
Each participant made two visits to the research laboratory. At the first visit, participants were randomly assigned a treatment order using a counter-balanced design based on their participant identification number. Participants were blinded to their treatment order. Treatments were separated by at least 48 hours and participants were instructed not to exercise for at least 4 hours before testing. We followed previous methods to measure the “stretching window” using intramuscular temperature in the triceps surae muscle group.10,11
During the experiment, participants lay prone on a treatment table and we visualized the greatest girth of the left triceps surae muscle group. From the posterior surface of this location, we measured and marked 1.2 cm down the medial side. The marked temperature probe insertion area was shaved, if needed, cleaned with an iodine swab, and wiped with a 70% isopropyl alcohol pad. The needle temperature probe was inserted horizontally into the triceps surae muscle group from the medial side. We verified the depth of the inserted temperature probe using musculoskeletal imaging ultrasound (LOGIQ e; General Electric Company, Chicago, IL). The probe insertion was deemed acceptable if it was within ±0.3 cm from the desired 1.2 cm depth. The receiving end of the temperature probe was plugged into the Iso-thermex and the electrothermometer was set to record the tissue temperature every 30 seconds.
Initial intramuscular temperature was recorded for 5 minutes, with the final temperature used as baseline as long as it was within ±0.5°C of the first value. We administered a 3-MHz ultrasound treatment over the posterior triceps surae muscle group at an intensity of 1.7 or 1 W/cm2, based on the participant's treatment order. A template was used to ensure that the therapeutic ultrasound treatment area was 10 cm2 (2× the size of the transducer used). Ultrasound gel (Aquasonic 100; Parker Laboratories, Inc., Fairfield, NJ) was used as a coupling medium during the treatment. During the treatment, we ensured that all participants felt warmth (yes or no question). The length of the treatment was recorded until the intramuscular temperature reached an increase of 5°C or more. The ultrasound treatment was stopped and temperature decay continued to be measured every 30 seconds until the intramuscular temperature reached the baseline value.
After all temperature recordings were completed, we removed the needle temperature probe, cleaned the insertion site, and applied an elastic bandage. The same procedures were used for both treatments, but the ultrasound intensity varied based on the participant's random treatment order. During the second visit, the needle temperature probes were inserted in the same area as the first visit (within 1 cm), but not in the exact same location.
We determined whether there was a difference in needle temperature probe depths between the two treatment conditions using a paired t test.
We calculated descriptive statistics for baseline and peak intramuscular tissue temperature, the time from the start of the treatment to an intramuscular tissue temperature increase of 5°C or more, the temperature decay time from peak to a decrease of 2°C or more and 3°C or more, and the time from peak to baseline intramuscular temperature.
We used paired t tests to determine whether the baseline and peak intramuscular temperature and temperature rise time to peak was different between the two ultrasound intensities. A 2 × 4 (intensity × time points 5′, 3′, 2′, and baseline) mixed design repeated measures analysis of variance was used to determine whether different temperature decay rates occurred between the high and low ultrasound intensities.
All data were pooled and a stepwise nonlinear regression analysis was used to create a prediction formula of temperature decay as a function of time following the ultrasound treatment. We used JMP Pro 12 software (SAS, Inc., Cary, NC) to analyze the data and the alpha level was set at a P value of .05 or less.
Two participants were unable to complete both treatment intensity sessions due to scheduling conflicts. Their data were removed from the data analysis because they were deemed incomplete for the cross-over design. All other participants completed both treatment sessions, for an 88.9% participant completion rate. No participants stopped the treatment early due to complications with the ultrasound device or sensations of uncomfortably hot tissue heating.
For all treatments, the needle temperature probe was placed at 1.23 ± 0.18 cm below the surface of the posterior calf in the triceps surae muscle and was not different between treatment intensity sessions (low intensity probe placement = 1.28 ± 0.17 cm, high intensity probe placement = 1.18 ± 0.18 cm; t30 = −1.507, P = .142).
There was no difference in baseline temperatures between the high and low intensity treatment conditions (t24 = −0.864, P = .369). The baseline intramuscular tissue temperature was 34.7°C ± 1.0°C and 35.0°C ± 0.9°C for the high and low treatment conditions, respectively. The high intensity treatment increased intramuscular temperature 5.3°C ± 0.2°C above baseline or to 40.0°C ± 1.1°C. The low intensity treatment increased intramuscular temperature 5.1°C ± 0.2°C above baseline or to 40.1°C ± 0.8°C. There was no difference in peak intramuscular temperatures between the ultrasound intensities (t30 = −0.757, P = .454).
The high intensity treatment (5.22 ± 3.37 minutes, 95% confidence interval [CI]: 3.43 to 7.01) created an increase of 5.0°C or more in the triceps surae muscle group faster than the low intensity treatment (9.66 ± 3.43 minutes, 95% CI: 7.83 to 11.49) (t30 = −3.691, P =.001). However, there was no difference in temperature decay times between the high and low intensity treatment conditions (intensity × time point interaction) (F2,60 = 0.057, P = .944). Time from peak intramuscular temperature to cool 2°C or more for the high and low intensity treatment conditions was 3.88 ± 2.53 minutes (95% CI: 2.53 to 5.22) and 3.97 ± 1.92 minutes (95% CI: 2.95 to 4.99), respectively. Time from peak intramuscular temperature to cool 3°C or more for the high and low intensity treatment conditions was 8.72 ± 6.98 minutes (95% CI: 5.00 to 12.44) and 8.09 ± 3.31 minutes (95% CI: 6.33 to 9.86), respectively. Time from peak intramuscular temperature for the tissues to cool back to baseline temperatures for the high and low intensity treatment conditions was 25.44 ± 11.8 minutes (95% CI: 19.12 to 31.76) and 25.72 ± 10.18 minutes (95% CI: 20.27 to 31.14), respectively. The treatment and temperature decay times are plotted in Figure 1.
(A) Time for intramuscular (IM) temperature to heat to ≥ 5°C above baseline during a 3-MHz therapeutic ultrasound treatment between two intensity conditions. Time for intramuscular temperature to cool (B) ≥ 2°C, (C) ≥ 3°C, or (D) return to baseline temperature from peak temperature after a 3-MHz therapeutic ultrasound treatment between two intensities. Mean and 95% confidence intervals bar graphs are plotted with scatterplot of individual participant data.
We found a significant nonlinear relationship between time and temperature decay (F3,1676 = 1.065, P <.0001, R2 = 0.70) and obtained the following prediction equation, where TD = temperature decay and t = time:
The heating rate and stretching window was previously measured with 3-MHz therapeutic ultrasound frequency. Our high ultrasound intensity condition had a similar treatment time (our results = 5.22 minutes) to previous research using an intensity of 1.5 W/cm2, which on average took 6 minutes to increase intramuscular temperature 5.3°C.11 Based on heating rates established using the same type of ultrasound device, a 3-MHz frequency with 1.0 W/cm2 to raise intramuscular temperature 5°C or more should take approximately 8.6 minutes.7 Our low intensity treatment condition took a minute longer (9.66 minutes) than the standard time, but this is not an unreasonable difference when using a different transducer, even from the same manufacturer.15
We found a longer temperature decay compared to previously published results. On average, it was previously found that it took 3.37, 5.83, and 18 minutes for the intramuscular temperature to decay 2°C, 3°C, and return to baseline temperature, respectively.11 When combining data from both therapeutic ultrasound intensities, we found that it took approximately 3.9 minutes (95% CI: 3.1 to 4.7), 8.4 minutes (95% CI: 6.5 to 10.3), and 25.6 minutes (95% CI: 21.7 to 29.5) for the intramuscular temperature to decay 2°C, 3°C, and return to baseline, respectively. Although it took longer in our study for intramuscular temperature to cool all the way to baseline, the stretching window time, when intramuscular temperature is greater than 3°C, was similar to the previously established time.
Different heating rates produced by different therapeutic ultrasound intensities did not alter the stretching window time. When a clinician's goal is to increase collagen elasticity and apply a range of motion technique immediately after the treatment, the intensity can be set to the patient's tolerance for heating. A higher intensity will create a shorter treatment time, giving the clinician more time for other rehabilitation techniques or to work with other patients. Based on our results, a clinician will save approximately 4.5 minutes per patient in therapeutic ultrasound treatment time if our higher intensity (1.7 W/cm2) is used instead of our low intensity (1.0 W/cm2).
Heat is dispersed away from the treatment area due to heat sinks and the three-dimensional volume of heating by the modality. As intramuscular temperature increases, local blood flow also increases, creating heat sinks to dissipate heat away from the tissues.16 Based on our temperature results, we hypothesize that the blood flow response is not altered by the rate of intramuscular tissue heating when heating the same treatment area, but is based more on the temperature change of the tissues. Although temperature decay rates are not altered by different heating rates when using the same modality, different therapeutic modalities will have different treatment area capacities. Therapeutic modalities that heat a larger three-dimensional area to the same intramuscular temperature (eg, pulse shortwave diathermy vs therapeutic ultrasound) will have a slower temperature decay. Thus, the tissue heat removal by heat sinks and heat loss mechanisms (eg, conduction) will be notably different between modalities.
Therapeutic ultrasound and range of motion techniques for muscle4,17 and inert tissues1,3 have created positive clinical outcomes. However, the research regarding the effects of therapeutic ultrasound and range of motion techniques on creating long-lasting tissue changes is severely limited. Two of these studies were conducted on healthy individuals and produced only acute gains after the interventions.4,17 Only one case study3 and one case series1 shows the clinical benefit of therapeutic ultrasound and range of motion techniques for pathological patients with tissue contractures. To our knowledge, there are no randomized control trials or systematic reviews conducted on this topic. Future high level clinical trials should determine the clinical effects of therapeutic ultrasound and range of motion techniques on patients with tissue contractures.
We measured the effects of two different therapeutic ultrasound intensities in muscle tissue, but therapeutic ultrasound has different absorption and heating rates in other tissue types. For example, when treating tendons, therapeutic ultrasound's heating rate has been two to three times faster than for muscle.18,19 It is hypothesized that therapeutic ultrasound has a faster heating rate in tendons because of its lower blood flow than muscle, limiting its ability to dissipate heat.18 Our results are limited to the application of different therapeutic ultrasound parameters to the stretching window in muscle. Future research should determine the stretching window properties in tendons and other tissues.
Our results are limited to the depth at which we placed the temperature probe into the tissue and ultrasound frequency that we used. Deeper tissues maintain their heat longer than superficial tissues.10,11 Thus, we would expect the stretching window to be longer in deeper tissues. Clinicians may decide to use a 1-MHz frequency to heat deeper tissues, but a 3-MHz frequency vigorously heated (Δ ≥ 4°C) muscle tissue up to 3 cm deep.20 The 3-MHz frequency heats tissues at a faster rate and decreases the necessary treatment time compared to 1-MHz frequency. However, future research could confirm whether 3- and 1-MHz therapeutic ultrasound frequencies would have similar temperature decay rates and stretching window times in deeper tissues.
We delimited our study by using the Omnisound 3000 ultrasound device, which has a higher heating rate than other therapeutic ultrasound devices.9,21 The higher heating rate is partially due to the transducer's better beam nonuniformity ratio used in our study compared to other devices.9 Different therapeutic ultrasound devices will likely have different heating rates to achieve the needed change in intramuscular temperature. However, based on our results, similar temperature decay rates, with different ultrasound devices, may occur once tissue temperature rises 5°C or more above baseline.
Other limitations of our study include the measurement method, participant population, and lack of range of motion techniques. We studied relative temperature increases in healthy, college-aged participants. Others have proposed that an absolute intramuscular temperature of 40°C needs to be reached to induce collagen elasticity changes.9 Intramuscular temperature in both groups did reach on average 40°C or more absolute intramuscular temperatures. We did not perform range of motion techniques during our study. Future research should continue to determine the effect of the stretching window prior to range of motion techniques in a clinical population.
Implications for Clinical Practice
A higher intensity ultrasound treatment will heat tissues faster to a state where collagen elasticity improves, but this faster heating rate does not alter the temperature decay rate. When targeting collagen elasticity changes before range of motion techniques, clinicians can set the therapeutic ultrasound intensity as high as feasible based on patient safety and comfort. A higher therapeutic ultrasound intensity will decrease the needed treatment time to reach the suggested temperature for changing collagen elasticity and potentially save the clinician time.
- Draper DO. Ultrasound and joint mobilizations for achieving normal wrist range of motion after injury or surgery: a case series. J Athl Train. 2010;45:486–491. doi:10.4085/1062-6050-45.5.486 [CrossRef]
- Nakano J, Yamabayashi C, Scot A, Reid WD. The effect of heat applied with stretch to increase range of motion: a systematic review. Phys Ther Sport. 2012;13:180–188. doi:10.1016/j.ptsp.2011.11.003 [CrossRef]
- Oates D, Draper DO. Restoring wrist range of motion using ultrasound and mobilization: a case study. Athl Ther Today. 2006;11:45–47. doi:10.1123/att.11.1.45 [CrossRef]
- Morishita K, Karasuno H, Yokoi Y, et al. Effects of therapeutic ultrasound on range of motion and stretch pain. J Phys Ther Sci. 2014;26:711–715. doi:10.1589/jpts.26.711 [CrossRef]
- Johns LD. Nonthermal effects of therapeutic ultrasound: the frequency resonance hypothesis. J Athl Train. 2002;37:293–299.
- Draper DO, Wells AM, Vincent WJ, Rigby JH. Ultrasound treatment temperature goals: temperature dependent versus time dependent. Athletic Training & Sports Health Care. 2013;5:76–80. doi:10.3928/19425864-20130213-01 [CrossRef]
- Draper DO, Castel JC, Castel D. Rate of temperature increase in human muscle during 1 MHz and 3 MHz continuous ultrasound. J Orthop Sports Phys Ther. 1995;22:142–150. doi:10.2519/jospt.1918.104.22.168 [CrossRef]
- Lehman JF, Warren CG, Scham S. Therapeutic heat and cold. Clin Orthop. 1974;99:207–245. doi:10.1097/00003086-197403000-00028 [CrossRef]
- Merrick MA, Bernard KD, Devor ST, Williams JM. Identical 3-MHz ultrasound treatments with different devices produce different intramuscular temperatures. J Orthop Sports Phys Ther. 2003;33:379–385. doi:10.2519/jospt.2003.33.7.379 [CrossRef]
- Rose S, Draper DO, Schulthies SS, Durrant E. The stretching window part two: rate of thermal decay in deep muscle following 1-MHz ultrasound. J Athl Train. 1996;31:139–143.
- Draper DO, Ricard MD. Rate of temperature decay in human muscle following 3 MHz ultrasound: the stretching window revealed. J Athl Train. 1995;30:304–307.
- Draper DO, Knight K, Fujiwara T, Castel JC. Temperature change in human muscle during and after pulsed short-wave diathermy. J Orthop Sports Phys Ther. 1999;29:13–18. doi:10.2519/jospt.1922.214.171.124 [CrossRef]
- Hawkes AR, Draper DO, Johnson AW, Diede MT, Rigby JH. Heating capacity of rebound shortwave diathermy and moist hot packs at superficial depths. J Athl Train. 2013;48:471–476. doi:10.4085/1062-6050-48.3.04 [CrossRef]
- Jutte LS, Knight KL, Long BC, Hawkins JR, Schulthies SS, Dalley EB. The uncertainty (validity and reliability) of three electrothermometers in therapeutic modality research. J Athl Train. 2005;40:207–210.
- Johns LD, Straub SJ, Howard SM. Analysis of effective radiating area, power, intensity, and field characteristics of ultrasound transducers. Arch Phys Med Rehabil. 2007;88:124–129. doi:10.1016/j.apmr.2006.09.016 [CrossRef]
- Ducharme MB, Tikuisis P. Role of blood as heat source or sink in human limbs during local cooling and heating. J Appl Physiol. 1994;76:2084–2094. doi:10.1152/jappl.19126.96.36.1994 [CrossRef]
- Draper DO, Anderson C, Schulthies SS, Ricard MD. Immediate and residual changes in dorsiflexion range of motion using an ultrasound heat and stretch routine. J Athl Train. 1998;33:141–144.
- Chan AK, Myrer JW, Measom GJ, Draper DO. Temperature changes in human patellar tendon in response to therapeutic ultrasound. J Athl Train. 1998;33:130–135.
- Draper DO, Edvalson CG, Knight KL, Eggett D, Shurtz J. Temperature increases in the human Achilles tendon during ultrasound treatments with commercial ultrasound gel and full-thickness and half-thickness gel pads. J Athl Train. 2010;45:333–337. doi:10.4085/1062-6050-45.4.333 [CrossRef]
- Franson J, Draper DO, Rigby JH, Johnson AW, Mitchell UH. Tissues at a 3-cm depth vigorously heat using 3-MHz ultrasound. Athletic Training & Sports Health Care. 2014;6:267–272. doi:10.3928/19425864-20141112-02 [CrossRef]
- Holcomb WR, Joyce CJ. A comparison of temperature increases produced by 2 commonly used ultrasound units. J Athl Train. 2003;38:24–27.