Participants

A total of 60 right-handed first year students participated in the study. These students practiced symmetrical sports (swimming, running, cycling, gym, roller-skating) as amateurs. All participants were tested for active rotation movements in the cervical spine. Two research groups were included in the study, depending on the angular values of the tested mobility. The experimental group (E; N = 22) comprised participants characterised by asymmetry in rotational movements. A difference of ≥10° (in absolute value) between right and left rotation of the cervical spine was considered asymmetrical. The control group (C; N = 38) included participants whose rotation difference was <10°. Both groups were divided into R1 and R2 subgroups due to the side of limited or less rotation. And so, R1 included people with limited (in the case of the control group ‐ smaller) right rotation, and in the R2 subgroup ‐ people with limited (in the case of the control group ‐ smaller) left rotation. The exclusion criteria included: age >21 years, pain in the cervical spine or shoulder girdle, any neurological symptoms in the area of the upper limb, operations in the area of the cervical spine or shoulder girdle, professional sports and practicing asymmetrical sports, scoliosis, any disorders of the physiological curvatures of the spine. A physiotherapist with over 10 years of professional experience supervised the proper course of the recruitment and diagnostics process. The characteristics of the study group are included in Table 1.

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Table 1. Characteristics of the study participants.

https://doi.org/10.1371/journal.pone.0298544.t001

Measurement methods

To perform the required angular measurements of the spine’s mobility, a Penny & Giles strain gauge electrogoniometer was used together with a Q110 single-plane sensor (Fig 2). The sensors were placed in the following anatomical regions: external occipital tuberosity (the lower edge of the upper sensor) and the spinous process of C7 (the upper edge of the lower sensor). The study assessed the angular values of the rotation of the cervical spine in both directions. Goniometric measurements were made in a sitting position. The measurement methodology according to Lewandowski [24] was used. Double-sided tape (Biometrics) was used to attach the sensors to the participant’s body. The result of the angular range of rotation (for each side) was the mean of three measurements performed directly in succession. The Penny & Giles strain gauge electrogoniometer is a reliable and repeatable measurement tool used to measure the segmental mobility of the spine [24].

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Fig 2.

Goniometric measurements of the cervical spine rotation in the starting position (left photo) and end range position (right photo).

https://doi.org/10.1371/journal.pone.0298544.g002

To assess the dynamic stiffness (S, measured in N/m) of the upper trapezius muscle, the MyotonPRO myotonometer by Myoton Muscle Diagnostics was used (Fig 3). Measurements were made on the upper trapezius muscle (right and left) at a point located in the middle of the section between the spinous process of the C7 vertebra and the acromion of the scapula (anterior apex, next to the acromioclavicular joint line). The participants were in the supine position. The probe of the device was placed perpendicular to the surface of the skin covering the examined muscle. Pattern composer had the following settings: tap time, 15 ms; interval, 0.8 s; mode, multiscan (five repetitions). MyotonPRO is a reliable and repetitive tool to measure the biophysical parameters of superficial soft tissues such as skin [25], muscle [26–28] or tendon [29]. The scientific literature indicates that this also applies to the upper trapezius muscle in the context of assessing dynamic stiffness [30]. MyotonPRO is reliable to assess biomechanical properties in a healthy population [31] and in people with pathological conditions [32,33].

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Fig 3. Stiffness measurement of the left upper trapezius muscle using MyotonPRO.

https://doi.org/10.1371/journal.pone.0298544.g003

Statistical methods

The sample size was determined on the basis of a previous study. Using the ’Power Analysis’ tool in Statistica 13.3 software (TIBCO Software Inc.; Palo Alto, CA, USA), the correlation coefficient (a variable calculated from previous studies), target test power and alpha value were substituted. A total of 9 cases were calculated, to yield at least 80% power of detecting an effect as statistically significant at the 0.05 α level, with a detectable effect size of 0.8.

The collected data on the range of rotational movement to the right and left as well as the stiffness of the right and left trapezius muscles were statistically analyzed in Statistica version 13.3

The normality of the distribution of the studied variables was checked with the Shapiro-Wilk test, and the equality of variances with the Levene test. To compare the stiffness values of the right and left trapesius muscles between the two groups (E and C), the Student’s t-test for independent samples or the Mann-Whitney test were calculated.

In order to determine the possible differentiation of the stiffness of the right and left trapezius muscles in the groups distinguished by: the presence of asymmetry in the area of rotational movement and the side of limited or less rotation, the analysis of variance with 4 levels (ER1, ER2, CR1, CR2) and post-hoc tests (LSD) with Bonferroni correction were applied, and Student’s t-test for independent samples or Mann-Whitney U test was calculated.

In order to investigate the effect of independent variables, i.e. right trapezius ST (R) and left ST (L) stiffness, on the dependent variables: the range of cervical right rotation (CRR) and cervical left rotation (CLR), the progressive stepwise regression was used.

Ethics

Participation in the study was free, voluntary and anonymous. It was possible to opt out of the study at any stage. Voluntary, written informed consent of the participants and the approval of the Bioethics Committee at the Poznan University of Medical Sciences (Number: 232/20) were obtained. The experimental procedures were conducted in conformity with the Declaration of Helsinki. The relevant guidelines and regulations of the local institute were strictly followed when conducting the study.

Research objectives and hypotheses

The main objective of the study was to answer the following question: is there a relationship between the stiffness of the upper trapezius muscle and the range of rotational movement of the cervical spine? The following research tasks aimed to answer this question:

1. determination of the differentiation of the stiffness of the right and left upper trapezius muscles depending on the occurrence of rotational movement asymmetry (differences between group E and group C) and the side of limited rotation (differences between groups ER1 and ER2 and groups CR1 and CR2);
2. determine whether there is a correlation between limited rotation and the stiffness of the upper trapezius muscle lying on the side of limited rotation and the stiffness of the upper trapezius muscle lying on the opposite side;
3. determine whether there is a correlation between the difference in right and left rotation and the difference in stiffness in the right and left upper trapezius muscle.

The following hypotheses were made:

1. There is a relationship between the stiffness of the right and left upper trapezius muscles and the range of right and left rotational motion of the cervical spine.
2. The upper trapezius muscle lying on the side of limited cervical spine rotation will be characterized by increased stiffness compared to the muscle on the opposite side.

Explanation of the results

We found that the stiffness of the right and left trapezius muscles depended on the location of the muscle related to the range of rotational movement. In the experimental group (asymmetry of rotational movements ≥10°), the muscles on the side of limited (less) rotation of the cervical spine were significantly stiffer than the muscles on the side of greater rotation. The statistical analyses showed that limited rotation of the cervical spine is associated with increased stiffness of the trapezius muscle on the same side. It is probably related to the function of the upper trapezius muscle. In addition to affecting the shoulder girdle, this muscle rotates the cervical spine in the opposite direction [34]. Contraction of the upper right trapezius causes the cervical spine to rotate to the left. In this way, the muscle on the opposite side is stretched. Hence, increased stiffness of the upper trapezius, resulting from limited stretching of this muscle, may limit cervical spine rotation.

Stiffness of the upper trapezius muscle in the experimental group did not differ significantly from the stiffness of this muscle in the control group (not showing asymmetry in cervical spine rotation to the right and left). The lack of a statistical difference in stiffness between the studied groups may be due to the fact that belonging to a given group was not determined by the value of the range of motion, but by the asymmetry of rotational motion. In the control group, there was no significant variation in upper trapezius stiffness depending on the side of rotation. However, in the experimental group with asymmetry of rotational movements, there was a variation in the stiffness of the upper trapezius muscle depending on the side of limited rotation, which allowed us to reject the null hypothesis. No articles describing the relationship of the stiffness of the upper trapezius muscle to the asymmetry of rotational movements of the cervical spine in healthy subjects were found in the literature. It is assumed that in the case of disturbances in the spinal parameters of the spine, this statistical difference could appear. Liang et al. [35] showed a significant effect of the position of the cervico-thoracic spine on changes in the stiffness of the upper trapezius muscle. The authors noted that the increased neck flexion angle significantly increased the stiffness of the examined muscle (p <0.05). Incorrect position of the spine in the cervico-thoracic section increased the stiffness in the upper, middle and lower part of the trapezius muscle. The authors conclude that correct posture is important in maintaining the reduced stiffness of the back muscles and may contribute to reducing the incidence of spinal overload syndromes [35].

The correlation coefficients indicate that right rotation of the cervical spine correlates most strongly with the stiffness of the right trapezius muscle (especially with the one lying on the side of less rotation), and left rotation correlates most strongly with the stiffness of this muscle on the left side (especially on the side of less rotation). In the conducted study, greater stiffness of the trapezius muscle more strongly reduced rotation in the side on which the muscle lies than rotation in the direction opposite of that muscle. This is probably related to the stretching mechanism of this muscle rather than its contraction.

Muscles often play different roles, acting as force-generating motors and brakes that dissipate mechanical energy [36]. In many cases, these functions are not mutually exclusive, and a single muscle often performs a variety of mechanically different tasks. Muscles with different mechanical functions act on different areas of the force-length curve [37]. Muscle operative length can be influenced by potential trade-offs between force production and sarcomere stability, while passive stiffness acts to limit the working length of the muscle [38]. It is believed that there is a significant relationship between the motor function of the muscle and its mechanical properties [38]. Increasing the passive stiffness of a muscle may limit its maximum operational length during movement [38]. In our study, we observed a reduction in the rotation of the cervical spine in a given direction (right or left), which was significantly associated with an increase in the stiffness of the trapezius muscle lying on the same side as the restriction of movement. This is explained in the above theory, since the right upper trapezius muscle is stretched during the rotation of the cervical spine, and the left trapezius muscle in the left rotation.

Influence of changes in muscle length on the stiffness parameter

There is evidence in the literature that changes in muscle length resulting from stretching or contraction significantly affect the stiffness parameter. Liu et al. [39] examined the stiffness of selected muscles of the lower limb in different settings of the knee joint and foot. In the case of passive stretching of the muscles (from the position of 50° plantar flexion of the foot to 25° dorsiflexion with the knee extended), there was a significant increase in stiffness [39]. For the gastrocnemius muscle, researchers found a 6-fold increase in this parameter in the area of the medial head and a 5-fold increase for the lateral head. The soleus muscle showed an almost 2-fold increase in stiffness, while in the proximal plantar fascia there was a 33% increase [39]. This phenomenon has also been confirmed in other muscles, including the tibialis anterior, tibialis posteriori, flexor digitorum longus and extensor digitorum longus [40].

Chang et al. [41] examined changes in the stiffness of the Achilles tendon depending on the foot position. The study was performed in a group of young, healthy participants. The authors noted that in the case of dorsiflexion of the foot (10°), the stiffness of the examined anatomical structure was clearly greater (p < 0.05) than in the case of setting the foot in the neutral position. This parameter increased by approximately 17%. The authors concluded that stretching the Achilles tendon increases its stiffness [41]. Tas and Salkin [42] confirmed the increase in Achilles tendon stiffness as a result of stretching. They noted a 40% increase in this parameter due to dorsiflexing the foot (10°). In turn, Aubry et al. [43] noted a 5-fold increase in Achilles tendon stiffness in the position of maximum dorsiflexion of the foot. The above scientific evidence shows that there is a relationship between muscle stretching position and increased stiffness. This applies to both muscles and tendons.

Several studies have shown a relationship between muscle contraction and an increase in muscle stiffness. In 2020, Yu et al. [44] reported changes in masseter muscle stiffness in a group of 20 healthy participants (10 women and 10 men). The mean stiffness of the examined muscle in the resting position was 369.5 N/m and it was 618.3 N/m at the maximum isometric contraction, for an approximately 67% increase in masseter muscle stiffness [44]. Kisilewicz et al. [45] investigated the effect of eccentric exercise on calf muscle stiffness in a group of 18 athletes. The authors noted a significant increase in stiffness (p < 0.001) due to the use of a single application of eccentric exercises (2 sets of 15 repetitions, 1 minute break between sets) [45]. The final measurement was performed immediately after the exercises. The authors noted a resting calf muscle stiffness of 323.5 ± 62.9 N/m and an increase in this parameter due to eccentric exercises to 392.7 ± 104.1 N/m [39]. Kelly et al. [46] assessed changes in stiffness depending on the strength of contraction (resting, 40% maximum voluntary isometric contraction [MVIC] and 80% MVIC) in the area of several muscles (infraspinatus, erector spinae and gastrocnemius). The authors noted an overall increase in stiffness depending on the strength of the muscle contraction. In the case of the infraspinatus muscle, the examined parameter increased by 46% at 40% MVIC and by 54% at 80% MVIC relative to the relaxed state. Erector spinae were characterised by a 31% increase in stiffness at 40% MVIC and by a 38% increase in stiffness at 80% MVIC. When examining the gastrocnemius muscle, the authors found a 45% increase in stiffness at 40% MVIC and a 50% increase in stiffness at 80% MVIC [46]. The above studies indicate that there is a clear relationship between muscle contraction and an increase in muscle stiffness.

Influence of stiffness on the locomotor system

Muscle stiffness is a biomechanical property of a tissue that represents the resistance of a muscle (tissue) to contraction or a deformation force [4]. Increased stiffness affects the function of a muscle as well as adjacent structures. It is believed that increased stiffness means greater effort from the antagonist is required to stretch the muscle. This leads to an increase in the energy cost of the movement, which is less economical for the locomotor system [4].

Some studies suggest that passive muscle stiffness may also have positive practical effects. Greater passive muscle stiffness (for a given joint angle) can contribute to the rapid build-up of strength [47]. This can be important in many sports and in the training process of players. More research is necessary in terms of the influence of increased stiffness and positive practical functional advantages.

There are reports of a relationship between increased muscle stiffness and pain in the head and cervical spine. Park et al. [48] examined the biophysical parameters of the suboccipital muscles and the upper trapezius in a group of 40 participants, half of whom had a cervicogenic headache. The authors noticed a markedly greater tonus and stiffness of the examined muscles in the experimental group compared with the control group (asymptomatic people). Suboccipital muscles were 20% stiffer, while the upper trapezius was 17% stiffer [48]. The authors suggested that their results should be taken into account in cervicogenic headache therapy [48]. Tas et al. [49] reached similar conclusions in a study focussing at neck muscle stiffness in patients with chronic neck pain. The authors noted significantly higher values of this parameter in relation to the upper trapezius, levator scapulae and sternocleidomastoid in patients with chronic neck pain compared to the control asymptomatic group [49].

Studies conducted on a group of people with chronic low back pain have also shown a relationship between dysfunction of the locomotor system and increased stiffness of soft tissues. Wu et al. [50] assessed the biophysical parameters of lumbar extensor myofascia in a group of elderly people with chronic low back pain. In the experimental group, the average stiffness of the dorsal extensor was 320 N/m, while in the control group it was 277 N/m [50]. The authors concluded that the mean stiffness of the dorsal extensor muscles was significantly greater in patients with chronic low back pain than in healthy controls. There was also a positive correlation between the level of perceived pain and the stiffness of the examined muscles [50]. Andonian et al. [51] also noted a markedly greater (p < 0.021) stiffness in patients with ankylosing spondylitis compared with the asymptomatic control group. The study concerned lumbar myofascia and the age range of the participants was 18–46 years [51]. The data from the study showed that people with ankylosing spondylitis much more often (p < 0.012) had lumbar myofascial stiffness greater than 250 N/m [51]. The above scientific reports indicate a relationship between disorders of the lumbar spine and increased stiffness of the soft tissues in this area.

Park et al. [52] noted an improvement in subjective, functional and biophysical parameters after posteroanterior mobilisation in a patient with ankylosing spondylitis. The authors noted a 2–4° increase in mobility [52]. Improvement in mobility in the sagittal plane was not statistically significant, but it was already present in the frontal plane. There was also a reduction in muscle stiffness in the cervical spine (the measurement was performed 2 cm laterally from the C4 spinous process) as a result of the applied mobilisation. The authors noted a 77 N/m decrease (20%) in this parameter. The treatment effect lasted for 5 days [52]. Although the study was only a case study, it shows a relationship between stiffness and mobility in the cervical spine area.

There have also been studies suggesting the need to reduce muscle stiffness as a form of prophylaxis and protection of the musculoskeletal system. Zhou et al. [53] conducted a study related to the evaluation of calf muscle stiffness after the use of static stretching. The authors indicated that greater stiffness of the Achilles tendon and gastrocnemius muscles is a risk factor associated with the occurrence of tendinitis. The authors suggested that heterogeneous behaviour is present within the gastrocnemius muscle and the Achilles tendon, and this heterogeneity is reduced after static stretching. They concluded that stretching can effectively increase muscle flexibility, resulting in better protection of the locomotor system [53].

Study limitations and future research directions

This study has several limitations. First, the observation was carried out on relatively small groups, which unfortunately was dictated by the concern for homogeneity of the study group. However, calculating the required sample size gave us acquiescence in the analyses and confidence that our results with a certain confidence level and assumed maximum error would estimate the true results in the population. Another limitation was the assumption of 10° for asymmetric right and left rotational movements. A larger difference between right and left rotation of the cervical spine between the study groups could indicate greater differences in the stiffness studied. The asymptomatic group is also a limitation to the study. Examining patients with pronounced cervical spine dysfunctions could allow more pronounced differences in stiffness to be captured in the intergroup analysis. A study assessing the stiffness of the upper trapezius muscle in the stretched position could also provide valuable information. It should be noted here that conducting such a study would be extremely difficult to carry out. It seems impossible to keep the active angular range of active rotation constant when performing stiffness measurements with MyotonPRO. We believe that in order to conduct such a study, the use of other research equipment should be considered.

In future studies, we plan to investigate the stiffness of the upper trapezius muscle in various ranges of mobility of the cervical spine. Evaluation of this parameter in groups of patients characterised by various dysfunctions of the musculoskeletal system should provide valuable data. Investigating the stiffness of several synergistic and antagonistic muscle groups while performing a given function could also be of scientific value.