Acute effect of resistance exercise at different velocities on stiffness and vascularity of the biceps brachii muscle: a preliminary study

Abstract

Background

Resistance exercise can be defined as the percentage of maximal strength (%1 repetition maximum) used for a particular exercise. Shear wave elastography (SWE) is a robust and novelty imaging technique that provides information regarding tissue stiffness. Superb microvascular imaging (SMI) is a non-irradiating technique that can provide quantitative measurement of muscle blood flow non-invasively.

Purpose

To compare the acute effects of low- and high-velocity resistance exercise on stiffness and blood flow in the biceps brachii muscle (BBM) using SWE and SMI.

Material and Methods

This prospective study included 60 healthy men (mean age=28.9 years; age range=26–34 years). BBM stiffness was measured by using SWE at rest, after low- and high-velocity resistance exercise, and muscle blood flow was also evaluated by SMI. Resistance exercise was performed using a dumbbell with a mass adjusted to 70%–80% of one-repetition maximum.

Results

The stiffness values increased significantly from resting to high- and low-velocity resistance exercises. There was no significant difference between the elastography values of the BBM after the high- and low-velocity resistance exercise. The blood flow increased significantly from resting to high- and low-velocity resistance exercises. Blood flow increase after low-velocity exercise was significantly higher compared to high-velocity exercise.

Conclusion

While muscle stiffness parameters and blood flow significantly increased from resting after both high- and low-velocity resistance exercises, blood flow significantly increased after low-velocity exercise compared to high-velocity exercise. This can mean that metabolic stress, an important trigger for muscle development, is more likely to occur in low-velocity exercise.

Keywords

Biceps brachii muscle resistance exercise shear wave elastography superb microvascular imaging muscle stiffness muscle blood flow

Introduction

Resistance exercise is a type of exercise performed with relatively heavy weights, with a small number of repetitions until the muscle reaches fatigue, and then ample time is allowed for rest and muscle recovery (1).

The results of studies on the effect of velocity of movement on hypertrophy and strength increase response of muscles in resistance exercise are contradictory. High-velocity resistance exercise has been shown to be more effective for muscle hypertrophy and strength than low velocity in eccentric contraction (2). On the other hand, some studies have reported that the increase in muscle cross-sectional area and muscle strength is similar in low- and high-velocity resistance exercises (3,4). In low-velocity exercise, muscle hypertrophy, myofibrillar, mitochondrial, and sarcoplasmic protein synthesis increased compared to high-velocity exercise at the same load (5,6). High-velocity exercises provide a good stimulus for neural adaptations (increased probability of doublet firing in individual motor units, motor unit synchronization), while low-velocity exercises increase metabolic stress and muscle tension, which are thought to be important factors in muscle hypertrophy (7). The blood flow of the muscle increases as contraction strength and workload increase and provides the needed metabolic muscle contraction (8). Increased blood flow during and after exercise is a complex event regulated by many factors. This blood flow is provided by the regulatory effect of central and local mechanisms. With increased sympathetic nervous system activation, the blood flow of the muscle is directed from the inactive tissues to the active muscles. Local control of the blood flow in the muscle during exercise is provided by the combination of muscle pump, O₂, K, hydrogen ions, lactate, adenosine, ATP, phosphate, osmolality, nitric oxide, free oxygen radicals, and vascular compression-induced rapid vasodilation (9,10).

Muscle hardness significantly increased with resistance exercise (11,12). Possible causes of this increase in stiffness are post-exercise muscle damage and muscle retention due to residual attachment between actin-myosin (11,12).

Shear wave elastography (SWE) is a new imaging technique that can evaluate the stiffness of soft tissues in real time and can be used to accurately measure muscle stiffness with this feature (13). In recent years, there have been publications evaluating the effectiveness of SWE in the musculoskeletal system (14 –17).

Superb microvascular imaging (SMI) is an early prototype in microvascular flow imaging providing extensive data on intralesion vascular networks. Using a high frame rate according to conventional Doppler techniques, such as color Doppler and power Doppler, SMI provides a clear view of thin vascular structures. Thanks to the ability of SMI to suppress scattering artifacts and to indicate slow flow signals, this modality can differentiate motion artifacts and small diameter vessels (18).

Muscle blood flow studies used conventional Doppler, microcomputed tomographic analysis, a gamma scintillation counter, or experimental modeling methods (19,20). However, in the literature review, there was no study in which acute circulation changes in the muscle were evaluated with SMI after muscle exercise. The aim of the present study was to measure the stiffness changes in the biceps brachii muscle (BBM) via SWE after resistance exercises and to evaluate the changes in the blood flow of the muscle with a new technology, SMI.

Material and Methods

Participants

A total of 60 men (mean age = 28.9 years; age range = 26–34 years) were included in this prospective study. All of the participants were untrained healthy young men, and none of them had a professional sports history. Since two participants could not tolerate and complete the exercises, the existing data were prepared according to 60 participants. The right arm was used in all participants because it was the dominant side. Individuals were not included in the study if they had a history of arm fracture, surgery, known history of musculotendinous injury, rheumatic, systemic, and/or connective tissue disorders, or chronic drug use.

The prospective study design and protocol were approved by the ethical committee of our institution (TÜTF-BAEK 2020/221). All individuals who participated in the study gave informed consent. This study was conducted at Trakya University Radiology Department between July and December 2020.

Study design

The BBM's stiffness and blood flow were measured while the participant was lying in a supine position on the desk with arms on the sides of the desk and parallel to the body. The forearms were also in the supine position. Participants were informed in detail about the sonographic examination to be applied, and they were asked to stay as relaxed as possible during the procedure. Measurements were made at the first application of the participants, after brief exercise and after long stretches of exercise, and all measurements were performed with an interval of five days. All measurements were made by a senior radiologist (FEU) with seven years of experience in SWE and two years of experience in SMI, and a junior radiologist (BSS) with one year of experience in SWE and SMI. Both observers performed the SWE and SMI evaluations in the same position, and the observers were not aware of each other's results. Both observers made all measurements twice to evaluate inter-operator reliability.

Shear wave elastography and superb microvascular imaging techniques

SWE measurements

All ultrasound (US) examinations were performed using an Aplio 500 Platinum US device (Canon Medical Systems, Japan) with a high-frequency linear transducer (frequency range = 7.2–14 MHz). The entire probe surface is covered with transmission gel, ensuring optimum image quality and minimizing the pressure of the transducer on the skin. The BBM was identified on the transverse imaging plane, and both SWE and SMI measurements were performed at this location.

Care was taken not to exact any pressure while applying the probe. During the evaluation, the screen was divided into two with a 2D-SWE map on the left side and quality mode on the right side. The quality mode, known as the propagation mode (arrival time contour), is a mode in which accurate data are obtained when the lines are parallel and smooth, while the increase in the distance between lines is proportional to the increase in stiffness.

The elasticity range was set to 0–80 kilopascal (kPa) on a standardized “musculoskeletal preset mode.” Thereafter, a 5-mm diameter region of interest (ROI) was placed within the elastography window to measure shear modulus data in kPa in the axial view (Fig 1). After three repeated acquisitions, mean elasticity and standard deviation values were used for statistical analysis.

SMI measurements

A pulse repetition frequency of 220–234 Hz and a frame rate >50 Hz were used in SMI measurements. A color box was placed with a fixed rectangular window within BBM. Next, the observer put a standardized (15 × 5 mm) ROI into the center of the BBM, and vascularity index (VI [%]), which represents the percentage of color pixels in the total grayscale pixels in a defined ROI, was automatically calculated (Fig 2).

All images were sent to and stored in our picture archiving system (Sectra PACS Linköping-SWEDEN).

Exercise protocol

The study procedure is shown in Fig 3. The biceps curl exercise with a dumbbell was used as the resistance exercise in this study. The biceps curl mainly targets the biceps brachii, brachialis, and brachioradialis muscles. BBM is stronger at elbow flexion when the forearm is supinated and weaker when the forearm is pronated.

The height and weight of the participants were recorded on the day they first applied. SWE and SMI measurements of the participants were then carried out before exercise, and the calculation of 1-RM of the muscle was started.

Calculation of 1-RM

The participant rested for 1 minute after performing 5–10 bicep curl repetitions at 40%–60% of the estimated 1-RM value . Then, by carefully increasing the weight, he performed the same exercise 4–5 repetitions again at 60%–80% of the estimated 1-RM. After each successful exercise, the participant rested for 3 min, and the weight continued to be increased until the person could no longer lift it. The highest weight the participant could lift at one time was recorded as 1-RM. It was aimed to reach 1-RM in a maximum of five trials [21].

Resistance exercises

The participant was called again five days after the 1-RM value was calculated. First, the participant warmed up with 5–10 bicep curl repetitions at 30%–40% of 1-RM value. Then, a high-velocity bicep curl exercise (2 s concentric / 1 s eccentric) was performed with three sets of eight repetitions with dumbbells weighing 70%–80% of the 1-RM value, which was the first of two types of exercise. The participant rested for 2 min between each set. Following the completion of the last set, the participant was placed on an US desk immediately, and the stiffness of the BBM was evaluated by SWE, and the blood flow measurement of the muscle was evaluated by SMI.

After five days, and after the abovementioned warm-up protocol, a low-velocity bicep curl exercise (8 s concentric / 4 s eccentric) was performed with dumbbells weighing 70%–80% of the 1-RM value, which is the second of the two types of exercise, was performed in three sets of eight repetitions. The participant rested for 2 min between each set. After completion of the last set, as after the first exercise, the participant was placed on the US desk without losing time, the stiffness of the BBM was evaluated by SWE, and the blood flow measurement of the muscle was evaluated by SMI. All exercises were performed under the observation of a sports doctor (FEA) with 10 years of experience in the profession, and the exercise and rest periods were timed with a stopwatch.

In order not to affect the measurements of the participants, the 1-RM value of the BBM and the measurements made after the high- and low-velocity exercise of the muscle were done on different days. All measurements were made between 09:00 and 10:00 in the morning. Participants did not perform heavy physical activity in the previous 48 h before measurement. Care was taken to ensure that the temperature of the ultrasonography room was around 25 °C throughout all measurements.

Statistical analysis

Statistical analyses were performed using the SPSS version 16.0 (SPSS, Chicago IL, USA). Quantitative variables were expressed as mean ± standard deviation and categorical variables as frequencies or percentages. Baseline data were evaluated using the Kolmogorov–Smirnov test, which showed that SWE and SMI values were normally distributed. Paired sample T test was performed between pre- and post-exercise SWE and SMI values to assess differences in elastographic and VI data.

Pearson's correlation coefficient was used to obtain the relationship between stiffness and blood flow parameters and to evaluate the relationship between elasticity and VI values. P values <0.05 were considered statistically significant. Inter-observer agreement in the quantitative analysis was calculated using intraclass correlation coefficients (ICCs) from a one-way random effects model analysis of variance, with the individual as the random effect. A 95% confidence interval (CI) was constructed for each ICC. ICC > 0.80 indicated excellent agreement.

Results

Descriptive statistics for elasticity and VI values obtained by two operators at rest and after high- and low-velocity resistance exercises are presented in Table 1. The body mass index of the participants was calculated as 25.7 ± 1.6 kg m². In the Pearson correlation analysis, SWE and SMI values after low-velocity exercise (r = 0.498; P = 0.025) were significantly correlated.

Shear wave elastography

Table 1.

Descriptive statistics of elasticity (kPa) and VI (%) obtained by two operators at rest and after exercises.

		At rest(n = 60)	After exercise(n = 60)	P value
Operator 1 (0 - short exercise)	Elasticity (kPa) VI (%)	7.62 ± 2.53 0.19 ± 0.19	10.63 ± 3.97 5.36 ± 2.01	0.017 <0.001
Operator 1 (0 - long exercise)	Elasticity (kPa) VI (%)	7.62 ± 2.53 0.19 ± 0.19	11.56 ± 6.1 6.32 ± 0.96	0.007 <0.001
Operator 2 (0 - short exercise)	Elasticity (kPa) VI (%)	7.95 ± 2.07 0.15 ± 0.15	10.47 ± 3.84 4.83 ± 1.45	0.015 <0.001
Operator 2 (0 - long exercise)	Elasticity (kPa) VI (%)	7.95 ± 2.07 0.15 ± 0.15	11.39 ± 2.86 6.17 ± 2.08	0.009 <0.001

Values are given as mean ± SD.

Statistical comparison between at rest and exercises with paired sample T test.

kPa, kilopascal; SWE, shear wave elastography; VI, vascularity index.

There was a significant increase in BBM stiffness compared to rest after high-velocity resistance exercise for both observers (P = 0.017 and 0.015, respectively). BBM stiffness was significantly increased compared to rest for both observers after low-velocity resistance exercise (P = 0.007 and 0.009, respectively). There was no statistically significant difference between the elasto values of BBM after high- and low-velocity resistance exercise (P = 0.251 and 0.223, respectively).

Superb microvascular imaging

There was a significant increase in BBM VI after high-velocity exercise compared to the rest for both observers (P < 0.001). After the low-velocity exercise, there was a significant increase in BBM VI compared to the rest for both observers (P < 0.001).

Comparing BBM VI values measured after high- and low-velocity exercise, the increase in VI after low-velocity exercise was significantly higher compared to high-velocity exercise for both observers (P = 0.022 and 0.029, respectively). Inter-operator reliability was perfect for the measurement of elasticity and VI at rest and after high- and low-velocity resistance exercises (range = 0.705–0.994) (Table 2).

Table 2.

Inter-observer variability for BBM measurements.

	ICC at rest(n = 60)	ICC after short exercise (n = 60)	ICC after long exercise (n = 60)
Elasticity (kPa)	0.941 (0.858–0.976)	0.974 (0.935–0.990)	0.984 (0.961–0.994)
SMI-VI (%)	0.948 (0.874–0.979)	0.968 (0.921–0.987)	0.872 (0.705–0.947)

Values are given as ICC (range).

BBM, biceps brachii muscle; ICC, intraclass correlation coefficients; kPa, kilopascal; SD, standard deviation; SMI, superb microvascular imaging; VI, vascularity index.

Discussion

To our knowledge, this is the first study in which acute stiffness and blood flow changes in the muscle were evaluated with SWE and SMI after resistance exercise performed at different velocities. The originality of the study comes from SMI, an innovative technique that effectively shows tissue vascularization. In addition, inter-operator reliability for SWE and SMI was also evaluated in this study.

A study by Caliskan et al. (22) evaluated the changes in the muscle with SWE and SMI as a result of the static stretching applied to the rectus femoris muscle, and this study is similar to ours because of the modalities used. However, it is inappropriate to compare these two studies since there are different mechanisms of muscle contraction and muscle stretching. A study conducted by Yanagisawa et al. (12) with strain elastography modality showed that BBM stiffness increased after resistance exercise compared to before the exercise.

A study by Akagi et al. (11) with SWE found that the stiffness of the triceps brachii muscle increased significantly after resistance exercise compared to before exercise. The increase in muscle stiffness after resistance exercise may be caused by the disruption of the distribution of Ca+² ions as a result of damage to the sarcomere membranes and the resulting shortening of the muscles (11,23,24). In addition, the increase in muscle stiffness can be explained by the shortening of non-contractile parallel elements of the muscle (25). In our study, in accordance with the results of the abovementioned studies, we showed that the stiffness of BBM increased significantly after the high- and low-velocity resistance exercises performed at high load (70%–80% 1-RM) compared to before exercise. The blood flow in the muscle matches the metabolic needs of contraction: as the contraction strength and workload increase, the blood flow of the muscle increases (8). Although there is no clear in vivo information, it is not surprising that the increased blood flow is useful for muscle structure. Increased blood flow provides better perfusion and increases the amount of oxygen and nutrition to the muscles, allowing for a higher level of physical performance (26).

In our study, after both exercise types, the increase in muscle blood flow was quantitated using SMI, and this increase was statistically significant. When we compare the two types of resistance exercises performed for short and long periods, it was seen that the increase in blood flow in the low-velocity exercise was higher than in the high-velocity exercise. This finding indicates that long-term resistance exercise performed at the same load creates more metabolic stress compared to short-term resistance exercise, and metabolic stress is an important trigger for muscle growth.

Muscle blood flow can be evaluated with different radiological modalities. In a color Doppler study conducted by Elvin et al. (27) using contrast media, they showed that the blood flow in the infraspinatus muscle decreased significantly in patients with fibromyalgia during exercise and immediately afterward, while the blood flow increased in volunteer participants. However, contrast-enhanced US is an invasive method as it requires intravenous contrast agent injection and may cause pain, anxiety, and allergic side effects in some patients. In addition, contrast agents used in US are not covered by public health insurance in Turkey. On the other hand, SMI is a risk-free modality that can be activated with a single button during the US procedure. It is easy to apply, cheap, and non-invasive, and it is an alternative that can be easily used in the evaluation of muscle blood flow.

Newman et al. (28) showed the ability of power Doppler sonography to evaluate exercise-induced changes in BBM blood volume. However, in the present study, the increase in muscle blood flow after exercise was evaluated qualitatively, and as in our study, evaluations with SMI will provide quantified results.

Laughlin et al. (29) showed that “muscle pump” is an important determinant of the perfusion of active skeletal muscle. It is concluded that during normal dynamic exercise, muscle blood flow is determined by skeletal muscle vascular conductance, the perfusion pressure gradient, and the efficacy of the muscle pump. Sheriff et al. (30) showed that dynamic exercise has a significant and immediate effect on conductance that cannot be explained by known neural, metabolic, myogenic, or hydrostatic influences. The aim of the present study was to make an objective evaluation by quantifying the blood flow after exercise using SMI. When we compared the two types of resistance exercise, which were performed at high and low velocity, we found that in the low-velocity exercise, muscle blood flow was higher, and there was no significant difference in elasticity between the two exercise types. Inter-observer variability of SWE and SMI were excellent (ICC range = 0.705–0.994) for the participant group in our study. We believe that this was achieved by the standardization of our technique as described in the “Materials and Methods” section.

The present study has some limitations. The main limitation is the narrow study population, which comprised only male adults. Therefore, there are no comments on the effect of applied techniques on gender. In addition, we do not know what the results will be when the same muscle measurements are made in the same way in the adolescent group. This is because the effectiveness of the contractile and non-contractile components of the muscle at different ages and hormonal changes varies. More comprehensive studies are needed on this subject. A secondary limitation is that only acute stiffness and blood flow changes in the muscle were measured after exercise. For this reason, it is not possible to comment on the subacute changes that exercise will create in the muscle. Finally, in Agaki et al. (13), different stiffness values were obtained with SWE in different parts of the triceps brachii muscle after exercise. We examined the central part of the BBM, and findings did not show what kind of change occurred in other parts of the muscle.

In conclusion, we can say that SWE and SMI are non-invasive and low-cost modalities that can be used to evaluate muscle stiffness and muscle blood flow before and after exercise, and it is thought to be widespread because it provides quantified values. In this study, we demonstrated with SWE that high- and low-velocity resistance exercise at high load (70%–80% 1-RM) leads to a similar increase in muscle stiffness. This result may be an indication that resistance exercise performed at different velocities against the same load causes a similar level of muscle damage. In the evaluation with SMI, we found that low-velocity exercise significantly increased the blood flow in the muscle compared to high-velocity exercise. We can interpret this result to mean that metabolic stress, which is an important trigger for muscle development, occurs more often in low-velocity exercise. However, further studies with larger groups of participants are needed to clarify this issue.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Fethi Emre Ustabaşıoğlu

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