Introduction
If exercise is increased to an intensity beyond that which is normally accomplished, it usually results in soreness that starts at about the first day after exercise and peaks at the third day after exercise. (13,45). This soreness, called delayed onset muscle soreness or DOMS, is characterized by a decreased range of motion of the joints (48), cellular inflammation (43), decreased muscle strength (24,26), and increased concentrations of intramuscular constituents in the plasma such as myoglobin (12,43,46). Delayed onset muscle soreness has been studied extensively and reviewed in numerous articles (5,21,46). Delayed onset muscle soreness can be quantified subjectively by analog visual pain scales (36,40) and objectively through blood analytes such as myoglobin and lactic acid dehydrogenase and cytokines such as IL1 and IL6 (35). Other objective measures include tissue resistance, thermography, range of motion of the joints, and algometry to sense muscle soreness (21,34).
Cold and heat have been used for thousands of years after exercise to reduce muscle soreness (42). Some studies purport that cold is the best modality immediately after exercise. Cold has been applied through cold packs, cold water hydrotherapy, and ice massage (10). The length and duration of the cold and the temperatures varies greatly as does the duration of the use of cold. Cryotherapy has been accepted as a means of reducing tissue damage and inflammation for many years and is usually used after sports-related injuries (29,32). Cold is used commonly on athletic teams such as for rugby players (38). However, research on the use of cold to reduce muscle microtrauma is sparse. The purpose of using cold is to reduce swelling and slow metabolism so that edema and injury are reduced (10). Cold also reduces pain and therefore has a duel role (10). However, the evidence is controversial. It is not surprising that numerous studies have either concluded no effect of cold or a good effect of cold on muscle soreness. Complicating matters even further, with lower-body hydrotherapy, many studies have shown that the body reacts with increased free radicals in the blood, potentially making matters worse after exercise with whole-body immersion (5).
Studies with the application of heat fare no better. Some studies use diathermy (7), some hot packs (1,29), and some ultrasound to warm the muscle after exercise (11). The use of heat also has 2 advantages. Heat increases metabolism in tissues (1,30,47). This should cause healing to occur more quickly (17,23). Another benefit of heat is that it reduces pain (14,22). But many heat modalities differ in their ability to penetrate into deep tissue. Hydrocollator hot packs, for example, are conventionally kept at 165° F (37). They are separated from the skin by 6–8 layers of towels (15). This reduces the heat that reaches the skin. Because they are left on for an average of only 20 minutes, in most people, there is no time for the heat to penetrate into deep tissue. This is especially compounded by body fat. If the subcutaneous fat is thick, then heat cannot penetrate in 20 minutes at all (15). Thus, for deep heating, hydrocollator heat packs, or similar devices used for brief periods offer pain relief to superficial nerves in the skin but not to deep tissue (15). The relief in deep tissue pain is probably due to gating on the dorsal horn of the spinal cord because of afferents from the skin responding to heat (2).
Other heat modalities, such as ultrasound, offer good penetration but are also used for brief periods of time (7). The same is true of warm water hydrotherapy, which is used for no more than 30 minutes and offers good heat penetration (41). For healing to occur, it seems logical that heat should be left on for hours and not just minutes. This can only be accomplished by low-level heat therapy. Only one paper examined low-level heat therapy after exercise with ThermaCare heat wraps and found them superior to cold, but heat was not applied until 18 hours after exercise and the measure of efficacy was subjective (3).
Therefore, in this investigation we used a subjective measure of soreness, an analog visual pain scale, compared to objective measures such as tissue elasticity, muscle strength, and blood myoglobin. Two modalities were tested; cold wraps compared to ThermaCare heat wraps, both applied either immediately or 24 hours after exercise that was at a high enough intensity to produce DOMS. The hypothesis was that cold modalities, by preventing swelling, would be better to reduce muscle damage and treat DOMS than heat or no thermal modalities used at all. Because some studies use cold and heat immediately, and others use these thermal modalities hours after the exercise, we subdivided the cold and heat groups into 2 subgroups—heat or cold immediately after exercise and cold and heat 24 hours after exercise.
Methods
Experimental Approach to the Problem
This was a balanced, randomized, between-group study design. Participants were randomly assigned to an experimental condition. The design involves 5 groups of subjects. One group was the control group and exercised and had all parameters measured during the study period. There were 2 heat groups, one that used heat immediately and another that used heat 24 hours after exercise. The same was true of the cold groups. The heat groups used a slow heat source that works for over 8 hours, whereas the cold groups used ice packs that, as per standard clinical practice, were left on for 20 minutes. The idea was to see if cold or heat used just after exercise would reduce muscle damage assessed by subjective and objective measures. The subjective measure was the visual analog pain scale, whereas the objective measures were tissue elasticity, blood myoglobin, and strength. Cold and heat were also used at 24 hours after exercise to see how they would compare to each other, as some studies use heat a day after exercise.
Subjects
The subjects in this study were 100 healthy individuals between the ages of 20 and 30 years (age range 20–29 years), divided randomly into 5 groups. The groups were (a) control, (b) cold pack immediately after exercise, (c) cold packs applied 24 hours after exercise, (d) heat packs applied immediately after exercise, and (e) heat packs applied 24 hours after exercise. All subjects did not participate in regular sports activities and were students at Loma Linda University. They had no training in squats or involving squats. All experiments were performed in March and April and all measures were conducted between 5 AM and 8 AM Subjects were almost equally divided between men and women, and the portion of men and women was the same in each group of subjects. All subjects were nonsmokers. The city of Loma Linda is a total smoke-free city. Their body mass index (BMI) was less than 40. Subjects had no cardiovascular disease, hepatic disease, diabetes, lower limb neuropathies, or recent lower limb injuries. Subjects were not taking alpha or beta agonist/antagonists, any type of nonsteroidal anti-inflammatory drugs, Cox 2 inhibitors, calcium-channel blockers, pregabalins (Lyrica; Pfizer Pharmaceuticals, NY, USA), or pain reducers. The demographics of the subjects are shown in Tables 1–5. There was no statistical difference between the ages, heights, and weights of the groups. All methods and procedures were approved by the Institutional Review Board of Loma Linda University in accordance with the Declaration of Helsinki, and all subjects signed a statement of informed consent.
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Table 1: Demographics of the control group.*
Table 2: Demographics of the cold immediately after exercise group.*
Table 3: Demographics of the heat immediately after exercise group.*
Table 4: Demographics of the cold after 24-hours group.*
Table 5: Demographics of the heat 24 hours after exercise group.*
Measurement of Muscle Strength
Muscle strength was measured with the subjects in the seated position with their leg held dependent. An ankle strap was connected from the ankle through a swivel joint to a stainless steel bar. The bar contained 4 strain gauges placed on opposite sides of the bar. When the bar was bent, the strain gauges, which were arranged as a Wheatstone bridge, were deformed, and an electrical output was provided to a BioPac (BioPac Systems, Goleta, CA, USA) system DAC100 bioelectric amplifier module. The signal was amplified 5,000 times and then digitized through a BioPac MP150 analog-to-digital converter at a resolution of 24 bits and a frequency of 1,000 samples per second, and stored digitally for later analysis (AcqKnowledge 4.1 software; BioPac Inc.). Maximum muscle strength was measured twice as a 3 seconds maximal effort, and at least 1 minute was allowed between contractions. The average of the 2 strength measurements was used in the data analyses as the subject's maximum strength.
Exercise
To induce DOMS, the subjects accomplished squats for 5 minutes. They squatted to the point where the hip was bent to 110° and the speed was set at 1 squat every 3 seconds. They repeated the exercise after 3 minutes of rest 2 more times (total 3 bouts). A coach participated with and observed the subjects to assure that they kept pace with a metronome.
Subjective Pain Measurement
A 10-cm horizontal line was drawn across a piece of paper. One end was marked “pain free” and the other “very, very sore.” The subject was asked to place a vertical slash across the line whereever appropriate. The location of the slash was converted into a number, where 0 indicated pain free and 10 indicated very, very sore. Only one visual analog pain scale was printed on a single sheet of paper.
Force to Flex and Extend the Knee
The force to flex and extend the knee was measured over a range of 90 to 125°. The subject was in the seated position with the leg dependent and supported off of the floor. A linear actuator was connected through an ankle strap to passively move the knee through 35° of flexion. The rate of movement was at 6°·s−1. The knee was flexed and then extended and the force was measured in each direction by 4 strain gauges. The bridge output was amplified and conditioned with a DAC100 strain gauge amplifier with a gain of 500 (BioPac Systems). The amplified output was digitized at 2,000 Hz with a resolution of 24 bits on an MP150 BioPac data acquisition system (BioPac Systems). A goniometer measured the angle of the knee. A complete description of this technique is given elsewhere (18,20).
Cold Therapy
Heat was applied by placing 1 ThermaCare cold wrap on each leg centered over the belly of the quadriceps and lying longitudinally over the muscle for 20 minutes.
Heat Therapy
Heat was applied by placing 1 ThermaCare heat wrap on each leg centered over the quadriceps and lying longitudinally over the muscle.
Blood Sampling
Approximately 5 ml of venous peripheral blood was collected from an antecubital vein using a disposable needle and vacutainer for serum or plasma with a serum separator, and whole-blood EDTA before and at 48 hours after exercise. The blood was placed in a refrigerated centrifuge and spun at 3,000 rpm for 10 minutes to separate the serum or plasma from the cells. The separated serum and plasma aliquots were stored at −80° C until analyses was conducted.
Plasma Biomarker Measurements
A Complete Blood Count was performed using a Mindray BC-3200 including the hematocrit and an automated 3 part white blood cellcount. For the measurement plasma myoglobin, commercially available enzyme-linked immunosorbent assay kits in a 96-well plate format, were used according to the manufacturers' instructions. (Plasma Myoglobin MG017C; CalBiotech, Spring Valley, CA, USA).
Procedures
On each day, subjects entered the room and relaxed in a thermally neutral environment for 20 minutes. Measurements such as leg strength and analogue visual pain scales were recorded. These data were collected on a Monday, exercise was accomplished on Tuesday, and measurements were taken again on Wednesday, Thursday, and Friday. This study consisted of 5 groups of subjects. The control group did not receive any modality. To study thermal modalities used immediately vs. 24 hours later, the experimental groups were divided into 4 groups, 1 group had ThermaCare heat wraps applied immediately after exercise and another group applied ThermaCare heat wraps 24 hours after exercise. Two groups either had cold treatment immediately after exercise or 24 hours after exercise. Wraps were placed on the long axis of the quadriceps bilaterally for 8 hours for dry heat and for 20 minutes for cold.
Statistical Analyses
Statistical analysis involved the analysis of variance and paired and unpaired t-test. The level of significance was p ≤ 0.05.
Blood analytes were measured and data corrected for changes in serum volume after exercise. First we corrected the hematocrit from venous blood to the true whole-body hematocrit, by multiplying the venous hematocrit value with 0.873. The change in plasma volume after the first day was then calculated, to correct for any shifts in plasma volume that would have impacted the concentration of analytes in subsequent measures (Figures 1–5). The formula we used is shown below.
where Ca = Final analyte concentration; Hct1 = Hematocrit on the control day; Hct2 = Hematocrit on the test day; Cb = Analyte test concentration (51).
Figure 1: The measured strength in the quadriceps muscles in the subjects before exercise (rest) and 1, 2, and 3 days after exercise. Each point is the mean of 20 subjects ± SD.
Figure 2: The measured visual analog pain scale of the subjects before exercise (rest) and 1, 2, and 3 days after exercise. Each point is the mean of 20 subjects ± SD.
Figure 3: The force required to passively move the quadriceps muscle with the knee at 110° in the subjects before exercise (rest) and 1, 2, and 3 days after exercise. Each point is the mean of 20 subjects ± SD.
Figure 4: The force required to passively move the quadriceps muscle with the knee at 110° during flexion minus the extension force in the subjects before exercise (rest) and 1, 2, and 3 days after exercise. Each point is the mean of 20 subjects ± SD.
Figure 5: Myoglobin in the control, heat, and cold groups. Each bar represents the average data on 20 subjects.
Results
Strength
As shown in Figure 1, there was a reduction in strength on the day after exercise in the control group. This significant reduction (p < 0.01) was 23.8% less than the resting (before exercise) strength. Both heat immediate and cold immediate groups also had a significant reduction in muscle strength of 4.5% by the first postexercise day and there was no significant difference between the groups, but both hot and cold application groups had significantly more strength than the control group on this day. The heat immediate group recovered by the second day after exercise to the pre-exercise strength, whereas the cold immediate group still showed a significant loss in strength at 3 days after exercise (p ≤ 0.05) compared to the pre-exercise strength.
When cold and heat were applied 24 hours after exercise, as shown in Figure 1, there was no statistical difference in strength between the 3 groups at rest or 1 day after exercise. The group that had cold applied after 24 hours appeared to recover their strength faster than the group with heat applied at 24 hours, with the slowest recovery in the control group. However, there was no statistical difference between the recovery in these 2 groups at day 2 or 3 after exercise (p = 0.4). Both groups had faster recovery than did the control group (p ≤ 0.05).
Analog Visual Pain Scale
The results of analog visual pain scale are shown in Figure 2. As can be seen in Figure 2, all subjects showed an increase in pain the day after the exercise. The pain peaked by 2 days after exercise. The least pain was felt 1 day after exercise and was in the heat immediate and cold immediate groups; there was no statistical difference between the hot and cold groups 24 hours after exercise. By the second and third day after exercise in the cold and heat immediate groups, the fastest recovery was observed in the cold immediate group.
For the cold and heat at 24 hour groups, there was no statistical difference between the control and heat at 24 hours groups. However, for the cold at 24-hour group, there was less pain 2 days after exercise than in observed the control group, as shown in Figure 2.
Force to Passively Move the Leg
The force needed to flex the knee was measured from the knee at 90–125°. Figure 3 shows the force that was measured at 110° of knee flexion. This measuring point was used because the measurement was well after the start of movement (90°) and when the inertia of the leg was brought to constant motion and was steady state. At this point, there were some differences in the forces to move the leg, depending on the leg length and girth of the leg from one individual to the next. Therefore, in this figure, all data were normalized in terms of the force to flex the knee before the exercise in each subject. There was no difference in the force to flex the leg one day after the exercise bout. In the group that had heat or cold immediately after exercise, the force stayed statistically constant over the next 2 days. For the group that had no heat treatment, force to move the leg increased significantly on the second and third day (p < 0.01). For the groups that had heat or cold applied 24 hours after exercise, the force was the same on the first, second, and third days after exercise (p > 0.05).
Figure 4 shows the hysteresis curve for the same measurement. The force to flex the knee at the 110° point and to allow it to extend to the 110° point is different. This difference is called the hysteresis. As shown in Figure 4, for the 4 groups that received heat and cold treatment, the hysteresis stayed constant over the 4-day period. But for the control group, there was an increase in the difference between the force of flexion and extension that peaked on the second day after exercise and was still significantly higher than the rest at the last day of measurements (p < 0.01).
The same was true for the heat and cold at 24-hour groups. Unlike the controls where hysteresis increased in the second and third day after exercise, for the heat and 24-hour–cold and 24-hour–heat groups it stayed constant over the 4 day period.
Figure 5 shows the change in myoglobin of the serum after exercise. The average myoglobin before exercise was 33.0 ± 4.6 micrograms per liter of blood. The largest increases in myoglobin were after dry, moist, and cold at 24 hours. These changes in myoglobin (% above rest in Figure 5) were significantly higher than the baseline but not different form each other. (p > 0.05) Heat and cold immediately did allow for an increase in myoglobin, but it was not significantly different than the resting data (p > 0.05).
Discussion
There is controversy as to the effectiveness of cold and heat after strenuous exercise (1,4,11,50). Some studies show that heat is better, whereas others favor cold, and others show little effect of either (5,16). The problem seems to be that when comparing heat to cold or examining either, there is no clear definition of what heat is or what cold temperature should be and the population of people being studied. Thus the literature is in total confusion. Another complicating factor is the duration of cold and heat. The issue is one of physics and heat flow. Warming the muscles to the core temperature is a slow process (27,33). First, subcutaneous fat buffers the gains in heat from the skin to the muscle (28,33). Second, basic heat flow equations show that the steeper the gradient the greater the heat flow (27). But if heat is too elevated above the core, the skin can burn (14,44). This limits rapidly applied heat modalities such as hydrotherapy to 20–30 minutes exposures (37). The same argument can be made for cold treatment except that cold can be tens of degrees less than the core temperature so that heat flow from the muscle can be more rapid. But there is still a vast difference in the tissue penetration of hydrotherapy vs. 50° cold packs vs. therapy ice packs separated from the skin by 6–8 layers of towels (37). Therefore, in this investigation, we used ThermaCare cold wraps (ice) directly on the skin for 20 minutes, and for heat treatment, we used ThermaCare heat wraps applied for 8 hours to standardize the heat and cold application. The 8-hour exposure allows the heat to gradually penetrate into deep tissue and keep it warm for hours. The exercise was standardized and all subjects were students with similar exercise training, age, and BMI so that variability in exercise and subjects could be eliminated to make a proper comparison of the effects of cold and heat.
Compared to the control subjects, who were very sore and lost a lot of strength after exercise, cold or heat both were both effective in reducing muscle damage and pain. Control subjects lost almost 24% of their strength in the days after exercise. The results show that to preserve muscle strength after strenuous exercise, heat immediately applied after exercise was best. In addition, using heat immediately after exercise seemed to result in the least damage to muscle, as assessed by myoglobin and the force of passive movement hysteresis curve. If heat and cold are not applied until 24 hours later, the reverse is true; cold is better than heat in preserving strength and reducing tissue damage.
This is supported by measuring the force needed to passively move the knee (18,19). Here, heat immediately after exercise caused the use of less force to passively flex the knee than it was found in the control subjects or after any of the other 3 modalities. Hysteresis in flexion and extension was increased in controls but was not increased if either cold or heat was applied to the legs immediately after exercise. This increase in hysteresis shows damage top muscle and soft tissue (18,19).
For reducing pain, the control subjects were very sore in the days after exercise. Cold immediately after exercise or 24 hours later was superior to heat in reducing pain, alhough both did reduce pain. Pain measured by a visual analog scale showed that soreness was reduced with cold immediately or at 24 hours and was more than it was found with heat, although both were superior in reducing soreness compared to the control subjects who did nothing.
The effect of heat and cold on pain is well documented. There are both voltage-gaited calcium hot and cold sensitive channels that interact with P2X2 purine channels that modulate pain in peripheral tissue (6,8,9). Although heat or cold is applied, the P2X2 pain receptors are inhibited and hence pain is reduced. But here pain was measured 24 hours after each modality and not during the application of heat and cold. In all probability, the effect on pain is caused by a reduction in tissue damage with heat or cold, causing less pain 24 and 48 hours after exercise. Strength data supports this fact, but the preservation in strength with cold and heat was best with heat, and pain reduction was greatest with cold. Therefore, there may be a carryover effect on pain seen here. Heat has been shown to have a carrier over pain relief 24 hours after heat is removed, (25,49) and perhaps there is some receptor inhibition for both heat and cold.
The difference in this study of cold and heat that allowed us to see benefits is that here we used a uniform exercise and subject population to test heat and cold. Mayer et al. (22) also used ThermaCare heat wraps but did not apply them until 18 hours after exercise. Their measure of effectiveness was subjective, and no hard measures were taken, although there seemed to be good results. Here objective and subjective measures were used; most previous studies of heat and cold used objective measures. In other studies, athletes were examined with ice baths. Ice baths with lower-body immersion seem to help, but they also cause a release of free radicals in the body, thus increasing whole-body inflammation. Further, in many studies lower-body cold immersion was for less than 5 minutes (5). This is not enough time for cold to penetrate into deep tissue (37). The same is true of contrast baths, which are too brief for either heat or cold penetration (31,39).
The results of this study however show what can happen with matched exercise and age of the subjects and condition of the subjects. Athletes, the elderly people, and people with diabetes may respond differently.
Practical Applications
For some reason in athletics, it is believed that cold after exercise is the best modality to prevent swelling and damage to muscle. At least for this age group, this is not true. There is a definite advantage of heat after exercise, if applied or used immediately. Cold and heat both prevent muscle damage, but on balance, heat actually has small advantages over cold in increasing healing after a heavy workout. The target population here was college undergraduate- and graduate-age students. Data would need to be collected on other population or even in this age range to examine these effects in athletes.
Acknowledgments
This work was supported by a contract from Pfizer pharmaceuticals under contract number WI173615.
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