Local passive heating administered during recovery impairs subsequent isokinetic knee extension exercise performance

Abstract

BACKGROUND:

Passive heating has attracted attention as a potentially promising recovery modality in sports. However, investigations of passive heating have yielded only inconsistent results for exercise performance.

OBJECTIVE:

To investigate the acute effects of local passive heating administered between repeated bouts of isokinetic exercise.

METHODS:

The experiment was a randomized crossover study. There was a total of three visits including a familiarization visit. During the remaining two visits, eleven healthy men performed three bouts of nine sets of isokinetic knee extensions using their dominant single-leg (30 repetitions/set, 180 ${}^{\circ}$ /sec). A 15 min recovery, during which a local passive heating pad at control (CON) or heating (HT) was applied to the rectus femoris, was afforded after the 3rd and 6th sets (Recovery 1 and 2). Isokinetic exercise performance, as assessed by peak torque, total work, and average power was analyzed using two-way repeated-measures ANOVA.

RESULTS:

Following Recovery 1 and 2, isokinetic exercise performance, as assessed by peak torque, total work, and average power was reduced in Set 4 ( $p<$ 0.001, $p<$ 0.001, $p=$ 0.080) and Set 7 ( $p<$ 0.001, $p<$ 0.001, $p=$ 0.009) in the HT group relative to the CON group. Electromyography analysis revealed that signal amplitude was lower in the HT group in Set 4 ( $p<$ 0.001) subsequent to Recovery 1, and that firing frequency was higher in Set 7 ( $p=$ 0.002) in the HT group after Recovery 2. Furthermore, EMG time-frequency maps from one representative participant showed that following Recovery 1 and 2 peak energy decreased during the first five repetitions in Set 4 and 7.

CONCLUSIONS:

Local passive heating administered during recovery decreased subsequent performance of isokinetic knee extensors, muscle activation ability and increased firing frequency maintaining force output. Therefore, local passive heating is not an appropriate acute recovery strategy for isokinetic exercises.

Keywords

Local passive heating isokinetic exercise recovery strategy exercise performance muscular strength

1. Introduction

It is well established that muscle temperature ( $T_{m}$ ) is a critical determinant of muscular strength and power. While increases in $T_{m}$ enhance muscular force and contraction speed, as well as improve exercise performance [1, 2], a decrease in $T_{m}$ delays the cross-bridge cycle and suppresses neuromuscular activity, among other effects, impairing performance [3]. Various warm-up strategies have been investigated for their potential ability to increase $T_{m}$ or maintain an elevated $T_{m}$ prior to a competition or during a recovery period [4].

A 1 ${}^{\circ}$ C increase in $T_{m}$ improves subsequent exercise performance by 2–5% [2, 5]. In some circumstances, the improved performance induced by the increase in $T_{m}$ induced is diminished, as when, for example, a 10–15 minute half-time break is provided (e.g. soccer or rugby) [6] or a 15–30 min transition phase between warm-up exercise and the beginning of a competition exists [4, 7]. This occurs because $T_{m}$ declines immediately upon exercise cessation [1].

Passive heating, which is feasible even in situations where active warm-up exercises are not, has received wide attention as a possible means of effectively maintaining elevated $T_{m}$ without depletion of energy substrates [4, 8, 9]. Various passive heating methods have been investigated, including hot showers, hot water immersion, heated athletic garments, and blizzard survival jackets [4]. As a post-exercise acute recovery modality, however, investigations of passive heating have yielded only inconsistent results. Passive heating has been shown to improve recovery from arm cycling and sprint [9, 10], such as decreasing the reduction of peak power output, sprint time or maintaining power output. The beneficial effects of increased $T_{m}$ have been explained as arising from its ability to amplify the rate of force development and power, muscle glycogen resynthesis, and neuromuscular activation [2].

In contrast, passive heating during recovery period failed to improve subsequent maximum voluntary contractions (MVC), submaximal squat performance, and grip strength [11, 12]. Pournot et al. showed that after two bouts of intermittent anaerobic fatiguing exercise, passive heating did not alter subsequent anaerobic performance [13]. Also, submaximal endurance cycling performance was not improved by passive heating as a recovery method between bouts of intense endurance cycling [14]. An in vitro study using an animal model revealed that passive heating for extensor digitorum longus muscle (EDL) between repeated muscle contractions led to more rapid fatigue [15]. Furthermore, Bailey et al. showed that passive lower-body heating decreased repetitive knee extensor exercise tolerance [16], a result that was explained as being a consequence of decreases in intramuscular phosphocreatine (PCr), pH, reduced glycogen accumulation as well as changes in neuromuscular activation [15, 16, 17].

Isokinetic exercise, which allows muscles to continuously gain strength throughout the range of motion, are a safe and effective means of rehabilitating muscles [18]. Isokinetic exercise training is also used to improve the muscular strength and endurance of athletes in many sports. Although isokinetic exercise is widespread, few have examined the effects of passive heating post-repeated isokinetic exercise. The aim of the present investigation was to investigate the effects of local passive heating administered between bouts of repeated isokinetic exercise.

2. Methods

2.1 Participants and ethical approval

This study was approved by Jeonbuk National University’s institutional review board (IRB#: JBNU 2019-09-010-002). Written consent of all the participants was obtained prior to the start of the experiment. The study conformed with the provisions of the Helsinki Declaration. Eleven healthy men from physical education department (Age: 30.7 $\pm$ 1.2 yrs, Body Weight: 82.5 $\pm$ 3.5 kg) participated in this study. All participants were healthy, free from medical illness, and had no upper or lower limb injuries. Participants who had a BMI $\geqslant$ 30 kg $\cdot$ m ${}^{-2}$ or had a history of any cardiovascular or metabolic diseases were excluded for this study. Participants were instructed to maintain their regular diet and physical activity during the experiment and were asked to refrain from high-intensity exercise, alcohol, caffeine, and carbonated drink consumption in the three days preceding their visit. The laboratory environment was maintained at 21–22 ${}^{\circ}$ C and 40–45% humidity.

Figure 1.

Experimental protocol.

2.2 Experimental design

The experiment was a randomized crossover study that included a total of three visits. On the first visit, participants were informed of experimental process, signed a written consent, and had their body composition measured (weight and fat-free mass) using an InBody 720 (InBody, South Korea) and have a familiarization session for isokinetic knee extension exercises (three sets of 30 repetitions, 180 ${}^{\circ}$ /sec) using their dominant single leg on an isokinetic dynamometer (CSMi, Humac Norm, USA). Each of the remaining two test visits occurred at the same time of day in random order with at least one-week separation between them (Fig. 1).

During the two test visits, each participant performed nine sets of 30 repetitions of dominant single-leg isokinetic knee extensions at a speed of 180 ${}^{\circ}$ /sec. A 90 sec rest was provided after each set was completed. After the first bout (Set 1–3) and the second bout (Set 4–6), a 15 min recovery period (Recovery 1 and 2) was provided, during which participants remained sitting on the isokinetic equipment and a customized tube-lined water-perfused pad (28 $\times$ 34 cm) was placed on the anterior thigh of the exercised leg. The pad’s temperature was maintained at 30 ${}^{\circ}$ C as control recovery (CON) based on skin temperature after the first bout of fatigue exercise and 40 ${}^{\circ}$ C for heating recovery (HT).

Neuromuscular activity was assessed by wireless electromyography (EMG; Trigno EMG Wireless, Delsys Inc., USA). Before attaching the EMG electrode, hair on the skin surface was shaved, disinfected with a 70% alcohol pad, and thoroughly dried. The EMG sensor was placed at 1/2 on the line from the anterior superior iliac spine to the superior part of the patella (i.e., rectus femoris).

Skin temperature ( $T_{\text{sk}})$ was assessed at two areas within the rectus femoris (moorVMS-LDF2, Moor Instruments, UK) before and after each set and averaged over 30 sec. Tympanic temperature ( $T_{\text{tym}})$ , an indirect index of core body temperature, was also measured using an infrared thermometer (IRT6520, Germany) to assess the effect of local heating on body temperature. All procedures were performed identically during each of the two test visits (i.e., CON and HT recovery).

2.2.1 Local passive heating

The local heating apparatus consisted of a customized pad (90% polyester and 10% spandex), a 40L heat-insulated container, a peristaltic pump, PVC tubes, a heating rod with a temperature controller, and a digital thermometer. The PVC tubes were lined up in parallel with each other within the pad. The temperature-controlled water in the container was pumped into the tubes of the pad by the peristaltic pump and was continuously circulated throughout the protocol. The temperature between the surface of the anterior thigh and the pad was monitored during the recovery phase using the digital thermometer to maintain a target temperature (i.e., CON and HT recovery).

2.2.2 Isokinetic exercise

Knee extensions were assessed using a dynamometer and Humac Norm software. The input arm was perpendicular and aligned prior to each test. After instrument calibration, the participant was seated in the adjustable chair and secured with safety straps around the waist and across the chest to limit position changes during the exercise. The ankle strap on the dynamometer’s lever arm was placed 2 cm proximal to the lateral malleolus. After the test, total work (Newton-meter, Nm), peak torque (Nm), and average power (Watts, W) per set, was calculated. Performance data was normalized to fat-free mass (kg) of the exercising leg for subsequent analysis.

2.2.3 Electromyography (EMG) measurement and analysis

Signals sent from the rectus femoris during the isokinetic exercise were wirelessly recorded with a sampling frequency of 2000 Hz. Mean frequency (MF) and root mean square (RMS) were calculated by analysis software (Delsys EMG Works Analysis 4.2.0, Delsys, Inc., USA). The filtering range was 10–500 Hz to reduce the noise in the low-frequency region and eliminate the motion artifacts in the high-frequency region. Because dynamic isokinetic contraction elicits larger peak EMG signals than maximum voluntary isometric contraction [19], EMG amplitude data during isokinetic knee extension exercises was normalized to the peak RMS in the first set of CON [20]. The threshold level was selected as 20% onset and 20% offset of the RMS [21]. Continuous wavelet transforms were performed for one representative participant (from 5th to 9th signal amplitude) using Morlet mother wavelet software by MATLAB with the signal processing toolbox (The MathWorks Inc., Natick, MA, USA) [22].

Table 1
Skin temperature ( $T_{\text{sk}})$ and tympanic temperature ( $T_{\text{tym}})$ . Data are presented as the mean $\pm$ SD ( $n=$ 11). ${}^{*}$ $p<$ 0.05, ${}^{**}$ $p<$ 0.01 vs. CON

		Pre Set1	Post Set 1	Post Set 2	Post Set 3	Recovery 1	Post Set 4	Post Set 5	Post Set 6
$T_{\text{sk}}$	CON	27.51 $\pm$ 0.9	27.70 $\pm$ 0.81	27.98 $\pm$ 0.83	28.51 $\pm$ 0.77	30.91 $\pm$ 0.65	30.20 $\pm$ 0.29	29.74 $\pm$ 0.27	29.79 $\pm$ 0.16
	HT	27.80 $\pm$ 0.79	28.25 $\pm$ 0.77	28.83 $\pm$ 0.53	29.04 $\pm$ 0.50	36.18 $\pm$ 0.43 ${}^{**}$	32.53 $\pm$ 0.30 ${}^{**}$	31.36 $\pm$ 0.59 ${}^{**}$	31.03 $\pm$ 0.53
$T_{\text{tym}}$	CON	36.45 $\pm$ 0.3	36.44 $\pm$ 0.41	36.30 $\pm$ 0.56	36.46 $\pm$ 0.43	36.53 $\pm$ 0.45	36.51 $\pm$ 0.3	36.41 $\pm$ 0.27	36.44 $\pm$ 0.39
	HT	36.53 $\pm$ 0.32	36.36 $\pm$ 0.40	36.33 $\pm$ 0.34	36.36 $\pm$ 0.35	36.31 $\pm$ 0.28	36.35 $\pm$ 0.39	36.40 $\pm$ 0.35	36.50 $\pm$ 0.39

		Recovery 2	Post Set 7	Post Set 8	Post Set 9	Effect
						Time	Group	Interaction
$T_{\text{sk}}$	CON	30.91 $\pm$ 1.13	30.18 $\pm$ 0.14	29.93 $\pm$ 0.17	29.73 $\pm$ 0.25	$F(11,33)=$ 107.1	$F(1,3)=$ 150.9	$F(11,33)=$ 16.81
	HT	36.00 $\pm$ 0.92 ${}^{**}$	32.85 $\pm$ 0.65 ${}^{**}$	31.85 $\pm$ 0.17 ${}^{**}$	31.36 $\pm$ 0.20 ${}^{**}$	$p<$ 0.001	$p=$ 0.001	$p<$ 0.001
$T_{\text{tym}}$	CON	36.50 $\pm$ 0.48	36.51 $\pm$ 0.22	36.41 $\pm$ 0.28	36.50 $\pm$ 0.37	$F(11,33)=$ 0.910	$F(1,3)=$ 0.277	$F(11,33)=$ 1.071
	HT	36.39 $\pm$ 0.29	36.30 $\pm$ 0.39	36.39 $\pm$ 0.27	36.43 $\pm$ 0.38	$p=$ 0.542	$p=$ 0.635	$p=$ 0.412

Figure 2.

Isokinetic knee extension exercise. (a) Total work, (b) peak torque, and (c) average power during each set of repeated isokinetic knee extensions are shown. Data are presented as the mean $\pm$ SD ( $n=$ 11). ${}^{*}$ $p<$ 0.05; ${}^{**}$ $p<$ 0.01; ${}^{***}$ $p<$ 0.001 vs. CON.

2.3 Statistical analysis

Data are expressed as mean $\pm$ SD, and statistical significance was accepted as $p<$ 0.05. Data was inspected for a normal distribution by Shapiro-Wilk test. Sample size was calculated based on our previous study [23] using G*Power software (latest ver. 3.1.9.7, Heinrich-Heine-Universität Düsseldorf, Düsseldorf, Germany). Variables were analyzed using two-way repeated-measures ANOVA, followed by a Sidak post hoc analysis; the factors were recovery conditions (CON and HT) and stage (Set 1–9) in isokinetic performance (total work, peak torque, and average power) and temperature data ( $T_{\text{sk}}$ and $T_{\text{tym}}$ ), and neuromuscular activity (RMS and MF). Absolute standardized effect sizes (ES, Cohen’s $d$ ) were calculated and reported in case of statistical difference between groups ( $d=$ 0.2, $d=$ 0.5, $d=$ 0.8 as small, medium, and large effects, respectively). Statistical analyses were performed using GraphPad Prism 9.2.0 (GraphPad Software, La Jolla, CA, USA).

3. Results

3.1 Changes in skin temperature (T ${}_{\text{sk}}$ ) and tympanic temperature ( $T_{\text{tym}}$ )

Changes in $T_{\text{sk}}$ and $T_{\text{tym}}$ throughout the protocol are shown in Table 1. As predicted, $T_{\text{sk}}$ was substantially higher after the 15 min recovery (Recovery 1) at HT than after the CON recovery ( $p<$ 0.001, ES $=$ 9.563). Following Recovery 1, the raised $T_{\text{sk}}$ steadily declined between Set 4 and Set 6 in the HT group, to the point that no group differences were observed during Set 6 ( $p=$ 0.051, ES $=$ 3.168). A similar pattern was observed between Recovery 2 ( $p<$ 0.001, ES $=$ 4.94) and Set 9. $T_{\text{sk}}$ , however, remained higher following Set 9 in the HT group than in the CON group ( $p=$ 0.003, ES $=$ 7.200). $T_{\text{tym}}$ remained stable in both groups throughout the entire test (Table 1, $p>$ 0.05 for all comparisons).

Figure 3.

Root mean square (RMS) and mean frequency (MF) from EMG. Changes in (a) RMS and (b) MF in rectus femoris during repeated isokinetic knee extensions are presented. Data are presented as the mean $\pm$ SD ( $n=$ 11). ${}^{*}$ $p<$ 0.05; ${}^{**}$ $p<$ 0.01; ${}^{***}$ $p<$ 0.001 vs. CON.

3.2 Isokinetic exercise performance

The passive heating groups tended to show attenuated total work, peak torque, and average power compared to the CON group (Fig. 2a–2c). For total work, there were significant time ( $F(8,80)=$ 23.04, $p<$ 0.001) and interaction effect ( $F(8,80)=$ 3.646, $p=$ 0.001) but not significant group effects ( $F(1,10)=$ 2.563, $p=$ 0.141). Peak torque showed significant time effect ( $F(8,80)=$ 16.82, $p<$ 0.001) and interaction ( $F(8,80)=$ 2.469, $p=$ 0.019) effects but not significant group effect ( $F(1,10)=$ 4.222, $p=$ 0.067). For average power, there were significant time ( $F(8,80)=$ 14.09, $p<$ 0.001) effect but not significant group ( $F(1,10)=$ 2.324, $p=$ 0.158) and interaction effects ( $F(8,80)=$ 1.514, $p=$ 0.166).

After the Recovery 1, total work was lower the HT group during Set 4 (CON 326.00 $\pm$ 53.64 vs. HT 287.92 $\pm$ 47.26 Nm/kg, $p<$ 0.001, ES $=$ 0.753) and Set 5 (CON 292.79 $\pm$ 46.07 vs. HT 266.35 $\pm$ 35.96 Nm/kg, $p=$ 0.004, ES $=$ 0.640) relative to the CON group (Fig. 2a). Following Recovery 2, similar reduction was detected in the HT group during Set 7 (CON 306.11 $\pm$ 54.07 vs. HT 257.78 $\pm$ 52.51 Nm/kg, $p<$ 0.001, ES $=$ 0.907) and Set 8 (CON 267.41 $\pm$ 40.23 vs. HT 242.84 $\pm$ 40.67 Nm/kg, $p=$ 0.009, ES $=$ 0.607).

After Recovery 1, peak torque was reduced in the HT group relative to the CON group during Set 4 (CON 12.82 $\pm$ 1.74 vs. HT 11.32 $\pm$ 1.59 Nm/kg, $p<$ 0.001, ES $=$ 0.900) and Set 5 (CON 11.52 $\pm$ 1.69 vs. HT 10.57 $\pm$ 1.35 Nm/kg, $p=$ 0.011, ES $=$ 0.621) (Fig. 2b). Following Recovery 2; significant reduction was observed in the HT group relative to the CON group during Set 7 (CON 12.00 $\pm$ 1.46 vs. HT 10.45 $\pm$ 1.83 Nm/kg, $p<$ 0.001, ES $=$ 0.936).

After Recovery 1, no difference in average power was detected between two groups during the second bout (Set 4: $p=$ 0.080, Set 5: $p=$ 0.245, Set 6: $p=$ 0.997) (Fig. 2c). Following Recovery 2, decreased average power was observed in the HT group during Set 7 relative to the CON group (CON 11.90 $\pm$ 3.31 vs. HT 10.44 $\pm$ 2.78 W/kg, $p=$ 0.009, ES $=$ 0.478).

Figure 4.

Representative time-frequency images computed by continuous wavelet analysis from one representative participant is shown (a–d). Energy was reduced following the 40 ${}^{\circ}$ C recovery (b and d) relative to the CON (a and c) both during Set 4 and 7.

3.3 EMG and time-frequency energy analysis

The time main effects (CON, and HT) for root mean square (RMS) and mean frequency (MF) in the EMG variables were presented in Fig. 3a and 3b. There were main time effects on RMS ( $F(8,80)=$ 23.44, $p<$ 0.001) and MF ( $F(8,80)=$ 11.99, $p<$ 0.001). Following Recovery 1, RMS was significantly lower in the HT group during Set 4 (CON 58.17 $\pm$ 7.40 vs. HT 48.80 $\pm$ 7.53 Hz, $p<$ 0.001, ES $=$ 1.255) and Set 6 (CON 52.12 $\pm$ 6.31 vs. HT 46.40 $\pm$ 7.88 Hz, $p=$ 0.049, ES $=$ 0.801) than in the CON group (Fig. 3a). No significant changes, however, were detected during the final bout (Set 7: $p=$ 0.393, Set 8: $p=$ 0.573, Set 9: $p=$ 0.999) following Recovery 2. MF was significantly higher during Set 7 in the HT group (CON 78.30 $\pm$ 12.55 vs. HT 83.95 $\pm$ 9.55 Hz, $p=$ 0.002, ES $=$ 0.507) (Fig. 3b).

Based on the EMG time-frequency energy map analysis, peak energy following the HT recovery was reduced during Set 4 and Set 7 compared to the CON recovery during Set 4 and Set 7, respectively (Fig. 4).

4. Discussion

In this study we evaluated the effect of local passive heating administered during recovery period on subsequent performance of repetitive isokinetic knee extensions. Our results showed that recovery with local passive heating (HT) reduced isokinetic exercise performance compared with the control group (CON), as assessed by reference to peak torque (Medium to large effect: ES $=$ 0.621 $\sim$ 0.936), total work (Medium to large effect: ES $=$ 0.640 $\sim$ 0.907), and average power (Medium effect: ES $=$ 0.478). Interestingly, isokinetic exercise performance decreased by 7 $\sim$ 14% relative to CON in the initial phases (Set 4 and 7) subsequent to the 15 min recovery periods in which local passive heating was administered (Fig. 2). During later phases of the exercise regime (Set 6 and 9), however, no discrepancy in exercise performance was observed between the two recovery groups, as reflected by changes in $T_{\text{sk}}$ that group differences in $T_{\text{sk}}$ disappeared in this later phase (Table 1). This may suggest that local heating is responsible for the reduced performance.

Similar to our study, Heinonen et al. utilized a water-perfused apparatus to locally heat calves, which increased $T_{\text{sk}}$ by $\sim$ 8 ${}^{\circ}$ C. In their investigation, intramuscular temperature increased from 33.4 to 37.4 ${}^{\circ}$ C, while core temperature was unchanged [24]. Based on our observed changes in $T_{\text{sk}}$ (i.e., increase by $\sim$ 8 ${}^{\circ}$ C from baseline), we assume that $T_{m}$ was elevated by approximately 4 ${}^{\circ}$ C. However, it is only speculation because heated regions as well as heating elements were different from their study.

Previous research concerning the relationship between acute passive heating and exercise performance has provided inconsistent data. Kilduff et al. reported that peak power output during countermovement jump (CMJ) and sprint performance were both higher relative to a control group when an increased core temperature was maintained with the aid of a blizzard survival jacket used during a 15 min recovery period [8]. The same research group also simulated a rugby game and showed that the administration of passive heat maintenance during a 15 min recovery decreased the decline of core temperature ( $-$ 0.74 $\pm$ 0.08%) compared to control ( $-$ 1.54 $\pm$ 0.06%), and has a positive effect on jump and sprint performance [9]. More recently, Cheng et al. investigated the relationship between intramuscular temperature ( $\sim$ 38 ${}^{\circ}$ C) and recovery from exhaustive endurance exercises in human and animal models, showing that elevating $T_{m}$ enhanced glycogen resynthesis and improved recovery [10]. Although heating methods are different from our study, it can be speculated that both core temperature and $T_{m}$ would affect exercise performance in above mentioned studies while core temperature did not seem to be affected by local passive heating in our study (Table 1). Also, types of exercise that was performed after passive warming may have been associated with the effect of passive heating (i.e., explosive vs. resistance exercise).

Contrasting studies have found that passive heating exerts no beneficial effect and may even impair subsequent exercise performance. Hot water immersion (HWI) at 44 ${}^{\circ}$ C for 60 min ( $T_{m}$ : $\sim$ 37 ${}^{\circ}$ C and skin temperature: $\sim$ 40 ${}^{\circ}$ C at 10 min) after resistance exercise did not improve MVC torque and submaximal squat performance [11] or 10-min hot shower after 30-min physical activity class failed to improve subsequent grip strength [12]. Also, recovery with temperate water immersion at 36 ${}^{\circ}$ C for 15-min following an intermittent fatiguing exercise did not provide any additional benefit to the performance of a maximal CMJ, MVC or a 30 s all-out rowing exercise performance when compared against the control recovery [13]. Crampton et al. also demonstrated that 30-min water immersion at 34 ${}^{\circ}$ C did not help maintain intense submaximal cycling performance throughout a second bout [14]. Furthermore, Bailey et al. showed that lower body HWI at 42 ${}^{\circ}$ C for 40 min increasing both $T_{m}$ ( $\sim$ 2.6 ${}^{\circ}$ C) and core temperature ( $\sim$ 0.6 ${}^{\circ}$ C) worsened repetitive knee extensor exercise performance (time to exhaustion) [16].

To determine the effect of heating recovery on muscular performance, two components must be considered: (1) changes in energy substrates such as glycogen or associated metabolites and (2) muscular function per se (i.e., force-generating ability and contractile speed) in response to heating.

Cheng et al. investigated the effect of a 2-hr recovery period in conjunction with passive local heating on arm cycling performance [10]. This treatment accelerated muscle glycogen resynthesis in response to heating, which consequently improved muscular endurance performance during a subsequent bout of exercise relative to the control. Other studies have determined that localized muscle heating accelerates glycogen synthesis during a subsequent bout of muscle contractions [25, 26]. Blackwood et al., however, recently showed that raising muscle temperature accelerates glycogen synthesis but inhibits glycogen accumulation as a result of the Pi-mediated phosphorylase activation [15]. Another study used magnetic resonance spectroscopy to reveal that HWI at 42 ${}^{\circ}$ C for 40 min ( $T_{m}$ increasing 2.6 ${}^{\circ}$ C , core temperature increasing 0.6 ${}^{\circ}$ C) impaired high-intensity knee extension exercise tolerance, though intramuscular PCr and pH decreased more rapidly, while Pi production sped up, in the heating group than in the control group during exercise [16].

We assessed muscular performance of approximately one min per set, which is largely dependent on the ATP-PC and anaerobic glycolytic system. Accordingly, lower intramuscular PCr, as well as $P_{i}$ -mediated inhibition of glycogen accumulation as a response to recovery with heating might have compromised subsequent isokinetic performance.

Muscle fatigue may also be due to the lower rate at which glycolysis provides ATP required to maintain muscular force [27]. Edwards et al. found that after single-leg immersion at 44 ${}^{\circ}$ C for 45 minutes, the endurance time of repeated isometric contraction of quadriceps was shortened at the highest temperature, and the utilization rate of ATP was only about 22% of total anaerobic sources [28]. Besides, under the muscle fatiguing protocol, in which the muscle fibers were stimulated at a constant rate, the time to peak twitch tension and half-relaxation time decreases when $T_{m}$ increases, such that the stimulation frequency should be increased to maintain muscular force output [29].

Together, these suggests that the subsequent reduction in isokinetic muscle performance caused by local passive heating during the recovery period in the current study maybe be due to the inhibition of the rate-controlling enzyme of glycolysis and a decrease in the rate of regeneration of ATP from anaerobic glycolysis required to maintain the contractility.

Myosin adenosine triphosphatase (ATPase) activity and Ca++ sequestration by the sarcoplasmic reticulum [30] increase along with muscle temperature, resulting in faster muscle contractions and higher rate of force development [3, 31]. Thus, previous studies assessing muscular power performance (e.g., sprints or CMJ) after the application of heating during recovery or pre-heating before competition, achieved positive results [8, 9]. In this study, however, muscular contraction speed was fixed at isokinetic 180 ${}^{\circ}$ /sec, ruling out the possibility that muscle contraction speed influenced muscular performance.

Muscle temperature elevation has been shown to improve contractile protein binding, thereby increasing muscle tetanic force [5]. While this improvement in force-generating ability has been observed in vitro animal model, raising muscle temperatures does not necessarily change peak twitch force in in vivo human skeletal muscles [31]. Accordingly, neither peak muscular force nor contraction speed seem to play a significant role in the results of isokinetic knee exercises performance following HT recovery. Rather, decreases in intramuscular PCr, pH; a reduction in glycogen accumulation and in the rate of regeneration of ATP from anaerobic glycolysis required to maintain the contraction are more likely responsible for the diminished performance of the isokinetic knee extensions [15, 16, 28].

In the current study, we observed that EMG RMS following the Recovery 1 was lower and EMG MF following the Recovery 2 was higher in the HT group relative to the CON group (Fig. 3). This was similar with a study by Thornley et al. who reported that the muscular endurance (time to fatigue) was reduced during isometric knee extensions after the anterior thigh muscle heated for 30 min ( $T_{\text{sk}}$ : $\sim$ 35.3 ${}^{\circ}$ C), and found that the average rectified amplitude decreased, and EMG MF was a downward trend over time, however, MF was higher than that in the control group [17]. The decrease in RMS may involve the accumulation of metabolites from the ATP hydrolysis, such as H+ or Pi, through small diameter afferents, resulting in an $\alpha$ -motoneuron inhibition and a reduction of supraspinal descending drive [32]. The elevated EMG MF was due in part to the increase in stimulation frequency required to maintain force output when $T_{m}$ is increased [28]. A representative wavelet time-frequency energy map showed that local heating during the recovery periods reduced the peak energy in the early stage (Set 4 and Set 7) of exercise (Fig. 4), which suggests the decrease of muscle space recruitment ability [22].

Overall, EMG analyses in the present study showed that local passive heating may lead to a decrease in muscle activation via an inhibition of motor neuron (Large effect: ES $=$ 0.801 $\sim$ 1.255) while MF is increased to maintain muscular force output (Medium effect: ES $=$ 0.507).

The present study shows that acute local passive heating administered during 15 min recovery impairs isokinetic exercise performance possibly due to attenuated neuromuscular activation. Alteration in muscle metabolism could be involved in the blunted isokinetic performance. Based on accumulated data, however, it seems evident that elevated muscle temperature increases muscle contraction speed and the rate of force development. Therefore, it is required to determine the effect of passive local heating on various types of exercise. Although speculative, local passive heating can provide performance benefit to exercises that require high explosiveness (i.e., muscle contraction peak speed or acceleration) such as jump or sprint. Future studies will be needed to determine the relationship between different levels of muscle contraction speed and performance following local passive heating in the same exercise model. Based on the current evidence, local passive heating as an acute recovery strategy should not be used for isokinetic exercises or exercises that primarily consist of isokinetic movement such as weightlifting.

4.1 Limitations

There are some limitations of the current investigation. We were unable to directly assess intramuscular temperature due to invasiveness of technique. We only speculate that $T_{m}$ was increased approximately by 4 ${}^{\circ}$ C based on a previous investigation [24] and future studies are warranted to determine changes in intramuscular temperature following local passive heating. Also, we could not blind participants for interventions because participants were able to recognize hot or control pads. There was a possibility that changes in exercise performance were influenced by a psychological factor (i.e., placebo effect) and therefore, studies with large sample size would be necessary to prevent bias and rule out a psychological factor.

We did not include female participants in the current study. It is well known that subcutaneous fat levels are different from different sexes [33]. It is speculative that conductive heat transfer to deep muscle tissues would be less in females than males. Therefore, interpretation of the present data should be limited to males. We were also unable to perform in-depth investigations of the molecular mechanisms that mediate the relationship between local heating during recovery and post-recovery performance. Additional research into the mechanisms that mediate this relationship are warranted.

5. Conclusions

We determined that 15-min of passive local heating administered during recovery reduced performance by 7 $\sim$ 14% during subsequent isokinetic knee extension exercises. Passive local heating also prompted an alteration in neuromuscular properties during isokinetic exercise, including EMG signal amplitude, firing rate, and motor unit recruitment. The collected data suggests that local passive heating is not an appropriate recovery strategy for isokinetic exercise. Further research will be required to determine whether local passive heating exerts any recovery effect applicable to other types of muscular exercise sufficient to warrant its utilization as an effective recovery therapy.

Author contributions

CONCEPTION: Yongling Chang, Xin Liu and Chansol Hurr.

PERFORMANCE OF WORK: Yongling Chang, Xin Liu and Chansol Hurr.

INTERPRETATION OR ANALYSIS OF DATA: Yongling Chang, Xin Liu and Chansol Hurr.

PREPARATION OF THE MANUSCRIPT: Yongling Chang, Xin Liu and Chansol Hurr.

REVISION FOR IMPORTANT INTELLECTUAL CONTENT: Yongling Chang, Xin Liu and Chansol Hurr.

SUPERVISION: Chansol Hurr.

Ethical considerations

Funding

This research was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (NRF-2019R1F1A1062693). This study was supported by the Research Base Construction Fund Support Program funded by Jeonbuk National University in 2021.

Footnotes

Acknowledgments

We thank each participant of this study. We would also like to express gratitude to the editors of the Writing Center at Jeonbuk National University for their skilled English language assistance.

Conflict of interest

None to declare.

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Local passive heating administered during recovery impairs subsequent isokinetic knee extension exercise performance

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSIONS:

Keywords

1. Introduction

2. Methods

2.1 Participants and ethical approval

2.2.1 Local passive heating

2.2.2 Isokinetic exercise

2.2.3 Electromyography (EMG) measurement and analysis

Table 1 Skin temperature ( T sk ) and tympanic temperature ( T tym ) . Data are presented as the mean ± SD ( n = 11). * p < 0.05, * * p < 0.01 vs. CON

3. Results

3.1 Changes in skin temperature (T sk ) and tympanic temperature ( T tym )

4. Discussion

4.1 Limitations

5. Conclusions

Author contributions

Ethical considerations

Funding

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Skin temperature ( $T_{\text{sk}})$ and tympanic temperature ( $T_{\text{tym}})$ . Data are presented as the mean $\pm$ SD ( $n=$ 11). ${}^{*}$ $p<$ 0.05, ${}^{**}$ $p<$ 0.01 vs. CON

3.1 Changes in skin temperature (T ${}_{\text{sk}}$ ) and tympanic temperature ( $T_{\text{tym}}$ )