59

Japanese Journal of Comprehensive Rehabilitation Science (2020)

Original Article

Effects of static and dynamic stretching of lower limb muscles on
oxygen uptake, heart rate variability, oxidized hemoglobin of
muscular blood vessels and muscular discharges during incremental
exercise
Takuya Ujikawa, RPT, MS,1,2,3 Tomoshige Koga, PhD1,2
Department of Physical Therapy, Faculty of Rehabilitation, Kawasaki University of Medical Welfare, Kurashiki,
Okayama, Japan2
Department of Rehabilitation, Graduate School of Health Science and Technology, Kawasaki University of
Medical Welfare, Kurashiki, Okayama, Japan3
Department of Rehabilitation Center, Kawasaki Medical School Hospital, Kurashiki, Okayama, Japan1

ABSTRACT
Ujikawa T, Koga T. Effects of static and dynamic
stretching of lower limb muscles on oxygen uptake,heart rate variability, oxidized hemoglobin of muscularblood vessels and muscular discharges during
incremental exercise. Jpn J Compr Rehabil Sci 2020;
11: 59‐64.
Objective: This study was conducted to clarify theeffects of three types of warming up (WU), namely
static stretching (SS), dynamic stretching (DS) andcycle ergometer riding at 20 watts (ergo), on
cardiopulmonary function and muscle activity during
incremental exercise.
Methods: Ten healthy adult males (aged 20.6 ± 0.5
years) participated in this study. Oxygen uptake, heart
rate variability, oxidized hemoglobin and dischargesof lower limb muscle were continuously recorded
during WU and the subsequently performed
incremental exercise.
Results: The sympathetic nervous activity index
analyzed from heart rate variability, oxygen uptake
and cardiac output significantly increased, and theparasympathetic nervous activity index decreased
after DS and ergo compared to those after SS.
However, no significant differences were foundbetween those values while exercise was maintainedat the anaerobic threshold level.
Conclusion: DS and ergo were suggested to be
Correspondence: Takuya Ujikawa, RPT, MS
Department of Physical Therapy, Faculty of Rehabilitation,
Kawasaki University of Medical Welfare, 288 Matsushima,
Kurashiki, 701‐0193 Okayama.
E-mail: ujikawa@mw.kawasaki-m.ac.jp
Accepted: February 25, 2020.
Conflicts of interest: The author have no conflict of interest
directly relevant to the content of this article.
©Kaifukuki Rehabilitation Ward Association 2020
doi.org/10.11336/jjcrs.11.59

effective for adapting to exercise, but these effects
seemed to disappear at the anaerobic threshold level.
Key words: static stretching, dynamic stretching,incremental exercise, heart rate variability, electromyogram
Introduction
Warming up (WU) is often performed to prevent
injury and achieve high kinetic performance. The
purpose of WU is to facilitate blood flow, increase
muscle temperature, and prevent muscular injury byincreasing the extensibility of connective tissue andmuscle elasticity [1]. Static stretching (SS) anddynamic stretching (DS) are often used as WU, whichis performed for the purpose of improving muscular
flexibility. The procedure of SS is as follows: thesubject slowly stretches the target muscle to the limitof the range of motion of the joint by themselves, andkeeps at the limit position for 20 to 30 s [2]. Becausemuscles are stretched without recoil in SS, signals
from the Golgi tendon organ suppress alpha motor
neurons in the anterior horn of the spinal cord via
inhibitory interneurons [3]. The stretch reflex seems tohardly occur since the muscle is slowly stretched, andmuscular tension is reported to decrease [2, 3]. In DS,
stretching effects can be obtained in the antagonisticmuscle by repeated flexion and extension. The target
muscles are repeatedly contracted without using recoil
to the final range of motion of the joint. In this way, thestretching effect of an antagonistic muscle is reported
to be obtained by reciprocal suppression [4]. Several
researches have been reported on the instantial effectof stretching. Noguchi et al. [5] reported that 2 min of
SS performed on the soleus muscle significantly
increased the dorsiflexion angle of the ankle joint andthat no significant difference in soleus muscle bloodflow was found. Fujibayashi and Nara [6] reported that
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Ujikawa T et al.: Effect of static and dynamic stretching on incremental exercise

DS, in which a hip joint flexion exercise was repeatedin the knee joint extension position, increased theflexibility of the hamstrings, and that muscular torqueand integrated value of the electromyogram weremaintained.
The anaerobic threshold (AT) calculated by thegradual increaseload exercise is the largest ● oxygen●
uptake (VO2) at which thebalance between VO2 and●carbon dioxide output (VCO2) is maintained, and is
known as an index of exercise tolerance [7]. Exercise
at the AT level is used as a prescription for exercise
therapy because it does not cause a significant rise inblood catecholamine or acidosis [8, 9]. It has beenreported that peak oxygen uptake (peak) obtained byincremental exercise is an indicator of prognosis inpatients with heart disease [7]. We examined theeffects of SS or DS of lower limb muscles on exercise
tolerance and the autonomic nervous system. This
study is considered to be significant in verifying theeffects of WU on incremental exercise at the AT levelor peak and circulatory risk management.
This study examined the effects of three types of
WU, namely SS or DS of lower limb muscles, andcycle ergometer riding at 20 watts, on oxygen uptake,ventilatory equivalent, heart rate variability, oxidized
hemoglobin of muscular blood vessels and musculardischarges during incremental exercise in healthy
adult males.
Methods
1. Subjects
The subjects of this study were 10 healthy adultmales (age 20.6 ± 0.5 years, height 168.3 ± 6.1 cm,
weight 62.8 ± 9.5 kg) without present illness or
medical history of respiratory, circulatory, or lower
limb locomotor disorders. Before the start of thisstudy, the subjects were explained the purpose andmethod of the study in writing and verbally, and agreed
by signature. This study was conducted with theapproval of the ethics committee of Kawasaki
University of Medical Welfare (approval number:
18‐063).
2. Methods
The subjects were asked to avoid taking alcohol andstrenuous exercise for 24 h and to fast for 2 h before
the experiment. They were interviewed about their
physical condition before the experiment, and they
participated in the experiment when problems were
not found.
2.1 Measurement items
Button-type disposable electrodes were attached tothe anterior chest to a lead electrocardiogram using awireless electrocardiograph (Trigno Wireless System,
Trigno). Sensors with three-axis accelerometers wereattached to the vastus lateralis and the lateral head of
Jpn J Compr Rehabil Sci Vol 11, 2020

the gastrocnemius muscle using a wireless transfer
type electromyograph (Trigno Wireless System,
Trigno). The attachment site was located at two-thirdsof the line connecting the anterior superior iliac spine
to the superior border of the patella in the vastus
lateralis muscle, and one-third of the line connecting
the caput fibulae to the heel in the lateral head of thegastrocnemius muscle [10]. A computer connected to
the Trigno Wireless System was used for recording,and the electrocardiogram and electromyogram wereanalyzed using LabChart (ver. 7 for Windows, AD
Instruments). Two probes were attached to the vastus
lateralis and the lateral head of the gastrocnemius
muscle, and the skeletal muscle oxygenation wasmeasured by spatially resolved spectroscopy usingnear-infrared spectroscopy (NIRS, multichannel tissue
oximeter Hb14‐2, ASTEM). The probes for NIRS
were attached near the sensor of the electromyograph,and the data were obtained using software (ver. 1.04
for Windows, Hb14). Data of the NIRS were adjusted
according to subcutaneous fat thickness measured
using an ultrasound diagnostic equipment (Prosound
SSD-3500SX, Aloka). The breath-by-breath methodof the respiratory gas analyzer (AT-1100A, ANIMA)
was used to measure expired gas concentration andventilatory equivalent, and the measurement data wererecorded by the AT-1100A software.
2.2 Study protocol
A cycle ergometer (Strength ergo 8, Mitsubishi
Electric Engineering) was used for the incremental
exercise. The height of the saddle was adjusted so thatthe heel was centered on the pedal when the pedal wasat the lowest point, and the knee joint was in theextended position. The position of the foot was set sothat the second metatarsal head was on the central axisof the pedal. The subjects performed WU for 4 min
and incremental exercise of 20 watts/min at the pedal
rotation rate of 60 rpm after resting for 3 min.
Incremental exercise was terminated when the pedal
rotation rate fell below 50 rpm over 3 s, or when thesubject informed that it was difficult to continue theexercise.
2.3 Types of warming up (WU)
Three types of WU for the incremental exercise
were employed in this study, namely (1) cycle
ergometer riding at 20 watts (“ergo”), (2) static selfstretching of the lateral vastus and lateral head of thegastrocnemius muscle (“SS”), and (3) dynamic
stretching of the lateral vastus and lateral head of thegastrocnemius muscle (“DS”). All subjects performed
the three types of WU in the experiment on different
days, and the order of the WU was randomly
determined. Each experiment was performed atintervals of at least 48 h to exclude the influence of
fatigue.
In “ergo”, the saddle height and foot position were61

Ujikawa T et al.: Effect of static and dynamic stretching on incremental exercise

the same as for the incremental exercise, and thesubject was asked to maintain riding at 20 watts at 60rpm for 4 min. The “ergo” was considered as thecontrol, since cycle ergometer riding is frequently
employed as WU before incremental exercise. In“SS”, the subject performed two sets of slow selfstretching for 20 s in order of the left quadriceps
femoris, the right quadriceps femoris, the left triceps
surae, and the right triceps surae muscle [11, 12]. The
stretching strength was controlled at the level to feelmoderate muscle tension without pain [13]. In “DS”
for the quadriceps group, the knee joint flexion andextension exercise was performed in an upright
posture while holding the hip joint in the neutral
position. In “DS” for the triceps surae muscle group,
the ankle plantarflexion and dorsiflexion exercise was
performed in the standing posture. One set of “DS”
was slowly performed five times, and then rapidly 10
times [2], and two sets were performed in order of thequadriceps femoris muscle group and the triceps suraemuscle group.

decreases significantly because the R-R interval
fluctuation is close to white noise during severe
exercise [15]. In this study, LF/HF and HF nu during
exercise above the AT level were excluded from theanalysis. The average value of oxygen hemoglobin(Oxy-Hb) recalibrated by subcutaneous fat thickness,
was used as an index of skeletal muscle oxygenation.
AT was determined by the V-slope
methodusing the●●calculated minute ventilation (VE) and V● O2/kg. The
stroke volume (SV) was calculated from VO2 and HR[16], and cardiac output (CO) was calculated from theproduct of SV and HR.

2.4 Measurement items and data analysis
One cycle of pedaling motion was determined fromthe value of the three-axis accelerometer, and the mean
power frequency (MPF) of the electromyogram during
three cycles was calculated, and it was considered as
an index of muscle fatigue [14]. The heart rate (HR),very low frequency (VLF) from 0 to 0.04 Hz, lowfrequency (LF) from 0.04 to 0.15 Hz, high frequency(HF) from 0.15 to 0.40 Hz, and total power (TP) from0 to 0.40 Hz were calculated by frequency analysis ofheart rate variability. The HF normalized unit (HF nu)= HF × 100 / (TP－VLF) was obtained by correcting
HF with TP and VLF, and was used as an index ofparasympathetic nervous activity, and LF/HF wasused as an index of sympathetic nervous activity. The
information about autonomic nervous activity

The experimental environment was a temperatureof 24.5 ± 1.2℃ and humidity of 44.8 ± 6.1%. In thisstudy, all subjects performed the three types of WU
and rode the cycle ergometer until oxygen uptake●
reachedpeak value (“peak”). The HR, LF/HF, VE,●
VO2/kg, and CO gradually increased as the incremental
exercise proceeded. Conversely, the HF nu gradually
decreased (Table 1, 2).

2.5 Statistical analysis
Statistical analysis was performed using software(SPSS ver. 22.0, IBM) and the significance level was
set at 5%. Friedman’s test was performed, followed by
the Wilcoxon signed rank test, and the results werecorrected by the Holm method.
Results

1. Parameter values during resting
We confirmed that no significant
differenceswere●●found in HR, HF nu, LF/HF, VE, VO2/kg, CO andOxy-Hb before the three types of WU (Table 1‐3).

Table 1. Comparison of heart rate variability between the three types of warming up (WU).

HR (bpm)

HF nu (nu)
LF/HF

rest
WU
AT
peak
rest
WU
AT
rest
WU
AT

ergo

SS

DS

75.1 ± 6.4
92.9 ± 6.5
115.6 ± 6.9
185.2 ± 13.4
52.1 ± 7.0
21.5 ± 7.4
6.3 ± 3.0
1.4 ± 0.5
3.2 ± 1.2
7.5 ± 3.1

75.1 ± 6.9
81.1 ± 7.1＊
108.2 ± 9.7
180.0 ± 16.1
55.2 ± 10.6
44.5 ± 10.1＊
8.4 ± 2.2
1.3 ± 0.2
1.7 ± 0.4＊
8.0 ± 1.3

73.2 ± 9.0  90.8 ± 8.8†
113.1 ± 8.9
187.6 ± 12.0
54.6 ± 3.9
19.3 ± 7.2†
7.2 ± 2.4
1.4 ± 0.3
3.0 ± 0.2†
7.5 ± 1.6

Mean ± standard deviation.
p < 0.05 ergo vs. SS, DS; †p < 0.05 SS vs. DS.
AT, anaerobic threshold; peak, peak oxygen uptake; SS, static stretching; DS, dynamic stretching;HR, heart rate; HF, high frequency; LF, low frequency.

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Ujikawa T et al.: Effect of static and dynamic stretching on incremental exercise

Table 2. Comparison of expiratory gas and ventilatory equivalent between the three types of WU.

●

VE (L/min)●

VO2/kg (mL/min/kg)

CO (L/min)

rest
WU
AT
peak
rest
WU
AT
Peak
rest
WU
AT
peak

ergo

SS

DS

7.0 ± 1.8
13.7 ± 1.9
24.3 ± 6.8
91.0 ± 24.7
4.0 ± 0.7
8.9 ± 1.4
17.9 ± 4.9
40.7 ± 6.8
3.7 ± 0.7
7.0 ± 1.0
10.9 ± 2.0
16.1 ± 2.6

6.9 ± 1.4
9.9 ± 1.6＊
24.8 ± 6.3
92.9 ± 26.5
4.4 ± 1.1
6.3 ± 1.1＊
18.1 ± 3.5
39.5 ± 3.5
4.0 ± 0.6
5.3 ± 0.9＊
10.9 ± 1.5
15.7 ± 2.2

6.6 ± 1.7
12.2 ± 2.6†
27.0 ± 7.0
97.9 ± 23.8
4.1 ± 0.8
7.6 ± 1.3＊†
20.5 ± 6.4
41.9 ± 6.2
3.8 ± 0.9  6.3 ± 1.2†
11.6 ± 2.1
16.7 ± 2.5

Mean ± standard deviation.
＊†p < 0.05 ergo vs. SS, DS;
p < 0.05 SS vs. DS.
●●
VE, minute ventilation; VO2, oxygen uptake; CO, cardiac output.
Table 3. Comparison of skeletal muscle oxygenation between the three types of WU.

Oxy-Hb (µM)
Vastus lateralis muscle
Oxy-Hb (µM)
Lateral head ofgastrocnemius muscle

rest
WU
AT
peak
rest
WU
AT
peak

ergo

SS

DS

39.0 ± 16.6
32.3 ± 10.0
36.2 ± 13.6
38.9 ± 13.9
50.1 ± 12.8
35.6 ± 9.9
43.6 ± 10.2
40.4 ± 11.6

39.7 ± 16.1  40.2 ± 14.4＊
38.7 ± 16.1
37.5 ± 12.8
42.5 ± 12.9  42.7 ± 12.4＊
37.7 ± 13.7
34.4 ± 10.0

41.2 ± 12.3
32.8 ± 9.4†
40.7 ± 8.4
38.6 ± 8.9
51.8 ± 15.4
34.6 ± 9.5†
43.7 ± 9.8
39.8 ± 12.5

Mean ± standard deviation.
＊p < 0.05 ergo vs. SS, DS; †p < 0.05 SS vs. DS.
Oxy-Hb, oxygen hemoglobin.
2. Comparison of parameter values just after thethree types of WU ●●The HR, LF/HF, VE, VO2/kg and CO showedsignificantly higher values just after ergo and DS
compared to those just after SS (p < 0.05, Table 1‐3).
Contrarily, the HF nu and Oxy-Hb of the vastus
lateralis and lateral head of the gastrocnemius muscle
showed significantly lower values just after ergo andDS compared to those just after SS (p < 0.05, Table
1‐3).
3. Comparison of parameter values after the three
types of WU at the exercise level of AT and peakoxygen uptake
To examine the effect of WU on exercise tolerance,
exercise loads at the AT level and peak oxygen uptake
were compared between the three types of WU. There
were no significant differences in both loads between
the three types of WU (Table 4). In addition, no
significant differences were found in any of the
Jpn J Compr Rehabil Sci Vol 11, 2020●●

parameters (HR, HF nu, LF/HF, VE, VO2/kg, CO,
Oxy-Hb and MPF) at both loads between the three
types of WU (Table 1‐3, 5).
Discussion
Stretching is generally employed as WU for
exercise. Although SS has been reported to have theeffect of improving muscle flexibility, it has beenreported that muscle weakness may occur temporarily[2, 3, 17]. DS has been reported to have the effect ofimproving muscular flexibility, maximum muscularstrength, knee extension power and agility [6, 18, 19].
It is important for circulatory risk management toexamine the effects of SS or DS of lower limb muscles
on motor function and autonomic nervous system ineach individual. In this study, we examined the effectsof SS or DS of lower limb muscles on oxygen uptake,heart rate variability, skeletal muscle oxygenation andfrequency of the electromyogram during incremental

Ujikawa T et al.: Effect of static and dynamic stretching on incremental exercise

63

Table 4. Comparison of work rate between the three types of WU.

Work rate (W)

AT
peak

ergo

SS

DS

85.0 ± 19.6
237.3 ± 42.4

82.5 ± 16.2
232.7 ± 43.6

87.6 ± 22.8
241.1 ± 45.9

Mean ± standard deviation.
Table 5. Comparison of frequency of the surface electromyogram between the three types of WU.

MPF (Hz)
Vastus lateralis muscle
MPF (Hz)Lateral head ofgastrocnemius muscle

AT
peak
AT
peak

ergo

SS

DS

72.2 ± 13.8
70.2 ± 7.5
117.9 ± 12.6
112.1 ± 32.5  76.1 ± 13.9  73.4 ± 13.5
111.9 ± 17.8
109.7 ± 21.0  79.4 ± 15.3  77.9 ± 14.5
108.8 ± 19.6
109.9 ± 33.1

Mean ± standard deviation.
MPF, mean power frequency.
exercise.
It has been reported that the load intensities
of ergo●and DS were higher than that of SS, since VO2, which
is an index that reflects the external load on the wholebody [20], after ergo and DS were higher compared●that after SS. After ergo and DS, the HR, LF/HF, VE
and CO values were higher and HF nu values werelower compared withthose after SS. Since it is known●
that HR, LF/HF, VE and CO increase and HF nu
decreases as exercise load increases, the load intensityof ergo and DS were considered to be higher than thatof SS. In addition, Oxy-Hb after ergo and DS showedsignificantly lower values than that after SS, indicatingthat peripheral oxygen consumption was increased byergo and DS. SS does not induce active muscle
contraction because signals from the stretched tendon
suppress the excitability of the alpha motor neurons,
thereby relaxing muscle tone [3]. Contrarily, the target
muscle is stretched by repeatedly contracting
antagonistic muscles and reciprocal inhibition in DS,
and the temperature of the muscle has been reported toincrease [21‐24]. Cycle ergometer riding (ergo) as
well as DS induce active muscle contraction, thus theload intensities of ergo and DS seemed to be higher
than that of SS. These results suggested that ergo andDS significantly cause respiratory and circulatory
activities, and skeletal muscle metabolism increases.
Furthermore, ergo and DS were suggested to have
preparatory effects for adaptation to exercise.
There were no significant differences in allparameters after the three types of WU at the exercise
level of AT and peak. It has been reported that theexercise of ankle plantar dorsiflexion increased HR
and LF/HF, decreased HF, and recovered 2 min after
exercise [25]. It has been reported that HR recovered
within 5 min after cycle ergometer riding at 75 watts[26]. These reports suggest that recovery after lowintensity and moderate-intensity exercise occurs
within 2 min and 5 min, respectively. In this study, theeffect of WU seemed to disappear at the AT level
exercise, because it took over 3 min to reach AT.
Furthermore, the incremental exercise might serve to
reduce differences among all parameters after the three
types of WU. These results suggest that ergo and DS
might have preparatory effects to enhance fitness to
exercise, however, a WU suitable for each individual’s
physical condition should be selected when performing
incremental exercise. This conclusion is based on the
result that no difference was found in the parameters inthis study when the exercise intensity reached the ATlevel. However, further study on risk management isrequired in the case of steady or hard load exercises.

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