Influences of Changes in the Level of Support and Walking Speed on the H Reflex of the Soleus Muscle and Circulatory Dynamics on Body Weight-supported Treadmill Training: Investigation in Healthy Adults (2024)

Abstract

[Purpose] To investigate the therapeutic usefulness of treadmill walking using a bodyweight support device (BWS), changes in circulatory dynamics and muscle activities withvarious levels of support were investigated. [Subjects and Methods] The subjects weredivided into 3 groups: 20% BWS, 40% BWS, and full body weight (FBW). The subjects walkedat maximum and normal speeds. Under each condition, H and M waves and skin temperaturebefore and after walking and changes in the heart rate during walking were measured.[Results] The heart rate continued to increase after 3 minutes of FBW at the maximumwalking speed, but a steady state was reached after 3 minutes under the other walkingconditions. Regarding skin temperature, no significant difference from that at rest wasnoted 30 minutes after walking at the normal speed, but it was significantly higher thanthat at rest at 30 minutes after walking at the maximum speed. The H/M ratio wassignificantly higher after walking at the maximum walking speed in the FBW and 20% BWSgroups compared with the 40% BWS groups. [Conclusion] Treatment with 40% BWS at themaximum walking speed was safe for the circulatory system and may be effective inelevating the skin temperature for a prolonged period compared with the effects of theother walking conditions at normal speed.

Key words: Body weight support, Walking speed, Skin temperature

INTRODUCTION

Many studies on treadmill walking using a body weight support (BWS) device for patientswith dysbasia have recently been reported. Werning¹⁾ and Dietz²⁾reported its usefulness in improving the walking ability of spinal cord injury patients in1992 and 1994, respectively, and walking speed-increasing and walking ability-improvingeffects were suggested. Studies on patients with hemiplegia^3,4,5,6), orthopedic disease^{7, 8)},cerebral palsy⁹⁾, and Parkinson’sdisease^{10, 11)} have also been reported, and body weight support treadmill training(BWSTT) is now widely applied.

The motor-physiological influence of BWSTT has also been investigated mainly in healthysubjects and stroke patients. Ohata et al.¹²⁾ performed electromyographic analysis of the lower limbs in BWSTTand observed that the action potential of the lower limb muscles decreased as the level ofsupport increased. A decrease in oxygen intake has also been reported as a markedBWSTT-induced change. Colby et al.¹³⁾reported that 20% and 40% body weight support decreased oxygen consumption by 6% and 12%,respectively. In a study using evoked electromyography reported by Osaka et al.¹⁴⁾, the maximum amplitude ratio of the H andM waves of the soleus muscle (H/M ratio) decreased after walking at 4 km/hour with andwithout support, and no significant difference was noted between the 2 groups. Since adecrease in the H/M ratio reflects the inhibition of spasm, the introduction of BWSTT may beuseful for hemiplegia patients¹⁴⁾.Although changes in the H/M ratio with an increase in walking speed have not yet beenclarified, the effectiveness of high-speed treadmill training in improving the walking speedwas noted in preceding studies on BWSTT for patients with diseases accompanied by paralysisand articular disease, such as hemiplegia and orthopedic disease^3,4,5,6,7,8). On the other hand, anincrease in the H/M ratio suggests the facilitation of motor cells in the spinal cord, whichmay be desirable to increase muscle strength for healthy individuals^{15, 16)}.

According to a report from the Japanese Society of Thermology¹⁷⁾, changes in the skin temperature after exercise arestrongly correlated with muscle blood flow and are useful in evaluating themicrocirculation. The gastrocnemius muscle is appropriate for blood flow evaluation usingthermography because it shows a strong reaction to exercise load and the muscle mass isrelatively large¹⁸⁾. Thus, to investigatedifferences in muscle blood flow among various BWSTT patterns, we measured blood flow in thegastrocnemius muscle using thermography.

No consensus has been reached with regard to the treatment protocol and indications ofBWSTT, and at present, they vary depending on the individual. However, for application ofBWSTT to actual clinical cases, it is necessary to clarify the physiological effect. In thisstudy, we compared the circulatory dynamics, skin temperature, and H/M ratio between BWSTTand full-body-weight treadmill training (FBWTT) in healthy adults with the aim of collectingbasic information to establish a treatment protocol for BWSTT.

SUBJECTS AND METHODS

The subjects were 45 healthy adults with no past medical history of neurological,orthopedic, or cardiopulmonary functional abnormality (33 males and 12 females, mean heightof 169.8±9.1 cm, mean body weight of 62.7±10.5 kg, mean age of 26.5±5.7 years).

Written informed consent was obtained from all the subjects.This study was performed afterapproval by the Ethics Committee of our hospital (approval number 24005). No potentialconflicts of interest were disclosed.

For body weight support, a harness-type device (BDX-UWSZ, Biodex Unweighting System, SAKAIMedical Co., Ltd.) was used. For the exercise, a treadmill (BDX-GTM3, Biodex UnweightingSystem, SAKAI Medical Co., Ltd.) was used. The trunk above the femoral region was coveredwith a vest that comes exclusively with this device, and this vest was lifted using wire todecrease the body weight loaded on the lower limbs while walking.

The weight load during walking was set at the full body weight (FBW) and 20% and 40% bodyweight support (20% and 40% BWS, respectively). The 45 subjects were randomly allocated tothese weight load conditions (FBW, 20% BWS, and 40% BWS groups; 15 subjects each) byemploying envelope methods (Table 1). Two conditions were used for the walking speed: the subjects were encouragedto continue walking as fast as possible, which was designated as the maximum walking speedunder one condition (Max), and to walk as usual, designated as the normal walking speed(Normal) under the other condition. All subjects walked barefoot at a constant speed undereach condition.

The subjects walked under the Max and Normal conditions in random order. The experiment wasperformed under one condition per day, and a 2-day or longer interval was set between theexperiments. The walking time was 6 minutes in all 3 groups, and changes in the heart rateand systolic blood pressure during walking were measured to judge whether respiratory andcirculatory reactions reached a steady state under each walking condition. In addition, theamplitudes of the H and M waves of the soleus muscle, H/M ratio, and skin temperature weremeasured before and after walking under each condition. To eliminate confounding factors,the maximum amplitude and skin temperature were measured under double-blinded conditions forthe examiner and subjects.

For measurement of the systolic blood pressure and heart rate, a noninvasive blood pressuremonitor (BP-203, A&D Company, Colin Med. Tech.) and a heart rate monitor (RS100TM,Polar) were used. Measurement was performed in a standing position, and the blood pressurein the right brachial artery was measured. The systolic blood pressure (SBP), heart rate(HR), and double product (DP = SBP × HR) were determined within 30 seconds or less beforewalking and at 3 and 6 minutes of walking.

The skin temperature measurement conditions were controlled at an atmospheric temperatureof 24±0.2 °C and humidity of 50±2%. The subjects wore short pants with both legs exposed,and were sufficiently acclimated to the room temperature at rest for 40 minutes. Formeasurement and recording, a thermography device (Handy Thermo TVS–200 ME, Nippon AvionicsCo., Ltd., Tokyo, Japan) was used. The skin temperature was measured on the posteriorsurface of the gastrocnemius muscle of the left crus. A rectangular frame with sides of 1/2the width of the popliteal fossa and 2/3 of the major axis of the crus was set on thegastrocnemius muscle, and the mean skin temperature in the frame was automatically measuredunder the following conditions: temperature step, 0.4–0.8 °C; temperature range, 6.4 °C;temperature step display, 16 steps; and number of frame additions, 32. Measurement wasperformed at rest, immediately after the completion of walking, and every 10 minutes for 30minutes after the completion of walking. In addition, the rate of change in the skintemperature ([skin temperature after walking − skin temperature before walking]/ skintemperature before walking × 100) was calculated.

For the measurement of H and M waves, an evoked electromyograph (Viking IV P 233 MHz,Nicolet) was used. After acclimation for a specific time using a plate electrode through theright soleus muscle, the impedance was adjusted to 5 kΩ or lower using a skinpreconditioning agent (skinPure, Nihon Kohden, Tokyo, Japan). The negative electrode wasfixed to the lateral side of the soleus muscle belly at about 1/3 from the periphery of thecrus, and the positive electrode was fixed to the Achilles tendon. Both electrodes werefixed using tape, and left on the leg until the completion of measurement after walking. Hand M waves were measured in the prone position. Regarding the stimulation conditions, thestimulus intensity was set at an intensity maximizing the amplitude, and the duration was0.2 ms. The tibial nerve was continuously stimulated 16 times through the right poplitealfossa with constant current rectangular waves at a stimulus frequency of 1 Hz and anintensity of about 1.1–1.2 times higher than the threshold of the H/M waves. The amplitudesof 16 waveforms (from the baseline to negative peak) were individually determined andaveraged. Measurement was performed at rest and 5 minutes after the completion of walking.In addition, the rate of change in the H/M ratio (H/M ratio after walking − H/M ratio beforewalking] / H/M ratio before walking × 100) was calculated after FBW, 20% BWS, and 40% BWS.To measure stable H waves, the subjects closed their eyes and mentally counted numbers toblock visual stimulation.

The measured values are presented as the mean±standard deviation. Subjects’ characteristicswere analyzed using one-way analysis of variance, with the level of support as a dependentvariable. For the nominal scale, the χ² test was used. One-way analysis ofvariance of the skin temperature was performed with the walking condition as a factor, thatof SBP, HR, and DP was performed with the time as a factor, and that of the evoked musclepotential was performed with the walking condition as a factor. In the subsequent analysis,the Bonferroni test was used for intragroup comparison, and Tukey’s HSD post hoc test wasused for intergroup comparison¹⁹⁾. Forcomparison of the H- and M-reflex amplitudes and H/M ratio between before and after walking,the paired t-test was used. SPSS Statics 21 was used for the statistical analysis and thesignificance level was set at less than 5%.

RESULTS

Under the FBW Max conditions, HR significantly increased until 6 minutes, not reaching asteady state at 3 minutes (Table 2). Under the other walking conditions, HR significantly increased in the first3 minutes of walking, but there was no significant difference between HR at 3 and 6minutes.

No significant change from the SBP before walking was noted at 3 minutes under the FBWNormal or 40% BWS Max conditions, but a significant difference was noted between the SBPs atrest and 6 minutes of walking. Under the FBW Max and 20% BWS Normal and Max conditions, theSBP significantly increased from that at rest in the first 3 minutes of walking, but nosignificant difference was noted between the SBPs at 3 and 6 minutes. Under the 40% BWSNormal conditions, no significant difference was noted in SBP among those at rest and 3 and6 minutes of walking.

DP significantly increased under the FBW Max conditions until 6 minutes, not reaching asteady state at 3 minutes. Under the other conditions, DP significantly increased from thatat rest in the first 3 minutes, but no significant difference was noted between the DPs at 3and 6 minutes.

The skin temperature on the posterior surface of the crus significantly rose with time thatat rest in the 10 minutes after walking under the Normal speed condition in all 3 groups andthen decreased to a temperature not significantly different from that at rest at 30 minutesafter walking (Table 3). Under the Max condition in the 3 groups, the skin temperature significantlyrose from that at rest in the 10 minutes after walking, and the temperature at 30 minutesafter walking was still significantly higher than that at rest. On comparison of the rate ofchange in the skin temperature, no significant difference due to the weight loadingcondition was noted at either the Max or Normal speed (Table 4).

In the evoked muscle potential measurement, the H- and M-reflex amplitudes and H/M ratiosignificantly increased after walking under the FBW Max and 20% BWS Max conditions (Table 5). No significant difference was noted in the rates of change in the H/M ratioamong the weight load conditions (FBW, 20% BWS, and 40% BWS) at the Normal speed (Table 4). At the Max speed, the rate significantlyincreased after walking under the 40% BWS conditions compared with those after walking underFBW and 20% BWS conditions.

DISCUSSION

The Max and Normal walking speeds were set by each subject in this study. The Normalwalking speed was slower than that in preceding studies (4 km/hour)^{14, 20)} because mostsubjects felt that walking at 4 km/h or faster was too fast and differed from their naturalwalking. Kubo²¹⁾ reported that the normalwalking speed on a treadmill is significantly slower than that on flat land due to theinfluence of sensation and familiarity. Finch et al.²²⁾ also reported that the normal speed of BWSTT decreased as the levelof support increased. In our study, the speed of BWSTT tended to decrease compared with thatof FBWTT, but the difference was not significant.

Regarding the SBP, HR, and DP, HR and DP continued to increase after 3 minutes under theFBW Max conditons, but a steady state was reached by 3 minutes of walking under the otherconditions. HR is widely used as an index of aerobic exercise in clinical physicaltherapy²³⁾. DP is strongly correlatedwith oxygen consumption of the myocardium and exponentially rises with a gradual increase inexercise. Thus, it is utilized as an index for indirect estimation of the load on the heartduring exercise²⁴⁾. Generally, factorsincreasing the SBP and HR during exercise include an increase in venous circulation due to areduction in the inspiratory intrathoracic pressure associated with muscle pumping andpromoted ventilation and an increase in the cardiac output induced by sympatheticotonia. Ina state-load exercise test, VO₂ reaches a steady state within 3 minutes when theload is smaller than the aerobic threshold (AT), and it exceeds 0 (at 3–6 minutes) when theload is AT or greater²³⁾. Therefore, underthe walking conditions other than FBW Max, the exercise load was lower than the AT andsafe.

In terms of the rate of change in the skin temperature, no significant difference was notedamong the weight load conditions, FBW, 20% BWS, and 40% BWS, at either the Max or Normalspeed, but the temperature at 30 minutes after walking at the Max speed was significantlyhigher than that at rest, showing that the temperature-elevating effect of the Max speedpersisted longer than that of the Normal speed.

In a study using thermography reported by Mori et al.²⁵⁾, repeated standing on the tips of the toes on one leg markedlyelevated the temperature of the gastrocnemius muscle on the motion side. They also directlystimulated an exposed feline gastrocnemius muscle preparation to confirm this musclecontraction-induced muscle temperature elevation, and it was shown that the muscletemperature rose immediately after stimulation and returned to the previous temperaturewithin about 30 minutes. In a study on the association between treadmill walking speed andlower limb muscle activity level using surface electromyography²⁶⁾, no significant change due to alteration in the walkingspeed between 2 and 5 km/h was noted in the muscle discharge level, but significantincreases were noted in the main muscles, such as the anterior tibial and gastrocnemiusmuscles, between 5 and 7 km/h, indicating that an inflection point of muscle activity duringwalking is present at about 5 km/h. In our study, the Max speed exceeded 5 km/h in all 3groups, suggesting that this change in the speed increased the gastrocnemius muscle activitylevel and led to the persistently high skin temperature.

No heat production resulting from sweating, tremor, or muscle tissue occurs at a roomtemperature of about 25 °C. Using thermography, the sympathetic function can be examined inthe temperature range of 20–30°C, and it has been reported to be useful in detectingabnormal sympathetic function accompanying pain²⁷⁾. Kanai et al.²⁸⁾randomly treated 69 patients with osteoarthritis of the knee using ultrasonic therapy andobserved that the skin temperature at rest significantly rose with the improvement ofsymptoms. The mechanism of pain relief by skin temperature elevation is due to improvementof blood flow, and it is considered that an increase in muscle blood flow removespain-inducing substances²⁹⁾. Therefore,the Max condition is effective in improving persistent pain after walking.

The H/M ratio increased after walking under the FBW and 20% BWS conditions at the Maxspeed, and the rate of change in the H/M ratio was significantly greater after walking underthe FBW and 20% BWS conditions at the Max speed than under the 40% BWS conditions at the Maxspeed. These findings support those reported by Yanagisawa et al.³⁰⁾: the soleus muscle H/M ratio linearly increasedimmediately after exercise when the weight on the lower limb increased. M waves are complexwaves induced by the excitement of α motor fibers, and they influence the size of H waves.Thus, the H/M ratio is considered to reflect changes in spinal cord α motor activitydirectly and accurately³¹⁾. H wavesdecrease for about 60 seconds after muscular activity due to inhibition by antagonist muscleand an increase in input by interneurons, but both H waves and the H/M ratio increase withdecreases in inhibition and input^{14, 32)}. In our study, the reciprocal inhibitionduring walking may not have influenced these parameters because measurement was performed 5minutes after the completion of walking. In addition, it was clarified that an increase inthe walking speed enhanced the excitability of spinal cord α motoneurons.

It was suggested that lower limb muscle tonus during walking training with BWS at the Maxspeed can be reduced by increasing the level of support. This condition may also be verysafe for the circulatory system as well as effective in elevating the skin temperaturecompared with that under Normal speed conditions.

The skin temperature rose immediately after walking under the BWS Max conditions, but thiswas an immediate effect. To generalize the findings, it is necessary to investigate thelong-term effect. In addition, to investigate the immediate effect in detail, investigationof kinesiological elements, such as muscle activity and articular movement, is necessary. Weused the heart rate as an index of energy consumption, but we did not measure the oxygenintake. In preceding studies³³⁾, theduration of H-reflex depression after exercise was markedly influenced by the level ofmuscle contraction force. We measured the evoked muscle potential 5 minutes after walking,but the validity of this time setting is unclear.

REFERENCES