Shear wave elastography of the upper trapezius muscle in patient with chronic neck pain: is there a correlation between elastic modulus and intensity of pain?

Background Chronic neck pain is a common discomfort and the alteration of elasticity of the upper trapezius in pathological conditions is unknown. Therefore, the aims of this investigation were (1) to determine the intra- and inter-operator reliability of evaluating the elasticity of the upper trapezius by shear wave elastography in individuals with chronic neck pain; (2) to examine the alteration for the upper trapezius during cervical flexion; and (3) to explore the correlation between elasticity of the upper trapezius and pain intensity. Methods Thirty individuals with chronic neck pain were recruited for this study. Alteration in elasticity of upper trapezius was evaluated by shear wave elastography during cervical flexion at 0°and 50°. Results The intra- and inter-operator reliability was excellent with the intraclass correlation coefficients ranging from 0.92 to 0.98. An increase of 30.80% was shown in the elasticity of the upper trapezius during cervical flexion of the painful side. In addition, there was a significant positive correlation between elasticity of the upper trapezius and intensity of pain (rho=0.647, P <0.05). Conclusion Shear wave elastography is a feasible tool for assessing changes of elasticity in muscles, and the findings in this investigation might be a good reference of evaluating upper trapezius elastic alterations in chronic neck pain.

in this area. The extensor muscles in the neck region play an important role in adjusting stability of the neck and shoulder 3 . Among them, the upper trapezius muscle contributes to normal neck and shoulder motion 4 . Recent studies reported that the patterns of activation and fatigue of muscles were disordered when people suffered from CNP 5-6 . Prolonged and unreasonable using of muscles also causes structural alteration of muscle including changed elasticity 7 . The alterations in the biomechanical properties of muscles might explain why patients feel discomfort in the neck region. However, to date the main methods for evaluating discomfort in CNP are palpation by physicians or the subjective perception of pain by patients. There is a lack of objective technology to assess the biomechanical properties of muscles in people with CNP.
Shear wave elastography (SWE), a novel technology, is increasingly applied to assess the biomechanical properties of muscles among healthy subjects and patients with musculoskeletal disease and has been shown to be a good reliability [8][9][10]. Our previous studies examining the elastic properties of the patellar tendon and quadricep muscle heads were also conducted by  In addition, there are reports that the SWE can evaluate the modulation of elastic properties of muscles. In a pathological condition, increased stiffness of the upper trapezius in athletes with rotator cuff tendinopathy could be assessed via SWE 10 . It was also detected that there were significant differences in elasticity of the biceps brachii muscles between the paretic and non-paretic side in stroke patients when using SWE 14 . Therefore, SWE is a feasible device with a high reliability to quantitatively evaluate alterations of elasticity in muscles in pathological conditions. People in certain professions such as computer and office workers have a higher risk of suffering from CNP. They usually sit for long periods with neck flexion at a fixed angle, which easily leads to discomfort and alteration of muscle fatigue [15][16]. The upper trapezius spanning the neck and shoulder is prone to structural muscle imbalance in poor posture. It has been reported that muscle metabolism is affected by trapezius myalgia, which it showed low local blood flow and insufficient oxygenation 17 . Comparing with changes of biochemical indicators, the elasticity of the upper trapezius might be impacted when people suffer from CNP. To date, no study has reported whether the elasticity of the upper trapezius in CNP is increased in poor posture. Therefore, it is necessary to assess the elastic modulus of the upper trapezius by SWE in pathological conditions. Additionally, muscle myalgia is a common symptom in neck pain. The visual analogue scale (VAS) is a relatively credible reference for assessing the intensity of chronic pain 18 . To our knowledge, no published data shows the relationship between pain intensity and elasticity of muscle with CNP. It is therefore important to confirm what kind of correlation exists between intensity of pain and elasticity of the upper trapezius in patients with CNP.
The objectives of this investigation were (1) to determine the intra-and inter-operator reliability of evaluating the elasticity of the upper trapezius by SWE in people with CNP; (2) to examine the alteration of the upper trapezius during cervical flexion; and (3) to explore the correlation between the elasticity of the upper trapezius and pain intensity.

Ethics statement
This study was approved by the Human Subjects Ethics of the Luoyang Orthopedic Hospital of Henan Province (KY2019-001-01). The trial protocol was conducted and kept by the Declaration of Helsinki. Each subject was informed about the procedures of the experiment and provided their written informed consent prior to the experiment before study.

Participant recruitment
Thirty patients (9 males and 21 females) were recruited from Luoyang Orthopedic Hospital of Henan Province through a recruitment poster on April 2019 and the trail was contacted from April to July. The inclusion criteria were (1) age (39.43 ± 14.34) years with chronic nonspecific neck pain, (2) only one-sided pain experienced in the neck region for > 3 months, (3) no therapeutic intervention before seeking medical advice, and (4) a score on the neck disability index (NDI) 5 [19]. The exclusion criteria were (1) other causes of neck pain such as cancer, fracture or neuropathy in the neck region and myelopathy, (2) neck surgery or clinical treatment for CNP, and (3) body mass index (BMI) > 30 kg/m 2 . In addition, authors had access to information that could identify individual participants during or after data collection.

Equipment of shear wave elastography
A novel device called SWE with an Aixplorer→ ultrasound unit (SuperSonic Imagine Aix-en-Provence, France) and a 50 mm linear ultrasound transducer (4-15 MHz) was used to evaluate the elastic modulus of the upper trapezius muscle. The principle of SWE technology is based on different shear wave velocity generated by pulses in various biological tissues [20]. Young's modulus, one of shear modulus, is generally used to indirectly reflect tissue stiffness, namely, E = 3ρv 2 , where ρ represents the density of the tissue 21 . The image of muscles is shown in B-mode and the parameter of elastic modulus is revealed in SWE-mode. Additionally, stiffer tissues were coded in red and softer areas in blue in SWE-mode 22 . The musculoskeletal mode was adopted to our one previous study for estimating the elastic properties of muscle with the temporal averaging (persistence), spatial smoothing set to medium and six, and penetration mode and the opacity at 85% 12 . The range of the colour scale was adjusted from 0 to 200 kPa.

Clinical evaluation
The parameters of pain intensity in the VAS were calculated in this investigation. Self-perceived pain which ranged from 0 to 10 points indicated intuitively the different degrees of intensity of pain [18]. The participants were required to assess self-perceived pain via VAS. Higher VAS scores revealed the worst pain and lower scores indicated the least pain 23 .

Procedures
Demographic information such as age, gender, weight, height, body mass index and weekly exercise hours were recorded before the experiment. All subjects were required to complete the assessment reports of NDI and VAS by themselves.

Measurement of upper trapezius elastic modulus
In the process of the difference analysis, the modulation of upper trapezius elastic properties was assessed by SWE during cervical flexion at 0° and 50° in the painful side.
The room temperature was maintained at 25 °C throughout all tests. All participants sat on a chair with shoulders in a neutral position and knees in 90-degree flexion. Before assessment, the subjects were allowed to have a 5 min rest in the sitting position. The angle of cervical flexion was measured by a new iPhone application named Goniometer Pro [24], which is a measuring tool of cervical spine range of motion with a good reliability 25 . Measurement sites were marked at the midpoint between the 7th cervical spinous process and the acromion using a marker 26 . Before scanning, ultrasound gel was applied to the skin around the probe location. In B-mode, the probe was placed perpendicularly to the skin and adjusted slightly for obtaining a clear image. Once the image without a muscle anisotropic artefact was determined, we switched to SWE-mode to quantify the elastic modulus of the upper trapezius muscle. (Fig. 1). The size of the circular regions of interest (ROIs) was defined as the thickness of the upper trapezius 7 Intra-and inter-reliability test The upper trapezius elastic properties in non-painful side were evaluated by SWE. The non-painful side was involved in the intra-and inter-operator reliability tests. The operators have extensive experience in assessing muscles elastic properties using SWE.
For assessing the intra-operator reliability, 8 subjects were examined by operator A using SWE at 0° of neck flexion. The same subjects were evaluated again by operator A 5 days later. For evaluation of inter-operator reliability, all subjects were assessed by both operators once, with a 30-minute interval. The operators were blinded to the results of measurements during the test. After completing the measurement task at each angle, participants were invited to relax for 2 minutes.
Statistical analysis SPSS Version 19.0 software (SPSS Inc, Chicago, IL) was used for data analysis. The demographic information was calculated by descriptive statistics. A paired t-test was performed to compare mean elastic modulus of the upper trapezius between 0° and 50° of cervical flexion in the painful side. The intra-and inter-operator reliability was determined by calculating intraclass correlation coefficient (ICC) with 95% CI. The intra-operator reliability was evaluated using the ICC (3,1) (two-way mixed effect model, consistency) and the ICC (2,2) (two-way random effect model, absolute agreement) was used to assess the inter-operator reliability. The standard error of measurement (SEM) was computed by the formula: SEM = standard deviation × , and minimal detectable change was calculated by the formula: MDC = 1.96 × SEM× . Bland-Altman plots further indicated the degree of agreement for evaluating reliabilities of SWE technique, which identifies the systematic error [27]. The correlation between elasticity of the upper trapezius and scores of the VAS was demonstrated by Spearman's rank correlation test. All measurement data were expressed as mean ± standard deviation, and P < 0.05 indicated a significant level.

Intra-and inter-operator reliability
The related statistical parameters involving intra-and inter-operator reliability in the nonpainful side during cervical flexion at 0° are revealed in Table 2 In addition, the Bland-Altman plots were exhibited in our study for further verifying consistency. As seen in Fig. 2, the 95% confidence limits, means and the distribution of points in plots were shown intuitively in picture, and all the points were within the 95% confidence limits. Therefore, the consistency in this investigation is satisfactory.

Alteration at different degrees of cervical flexion
There was an augment of 30.80% in elasticity of the upper trapezius in the painful side with neck flexion in this investigation, of which the average values were 62.84 ± 13.80 kPa at 0° of cervical flexion and 90.75 ± 19.94 kPa at 50°. This is the first study to estimate alterations of elasticity of muscle in patients with CNP. There are insufficient data in published studies to make a comparison. Comparing with data in healthy individuals (17.11 ± 65.82 kPa), the elasticity of the upper trapezius in this study was stiffer, which was a significant increase of 72.77% [31]. Moreover, one study assessing the upper trapezius with myofascial trigger points indicated that the mean of shear modulus was 13.56 kPa at rest position and a significant difference was found compared to our study Correlation between elastic modulus of upper trapezius and pain intensity One of the main findings from this investigation was a significant positive correlation between elastic modulus of the upper trapezius and intensity of pain, which the stiffer muscles, the greater intensity of pain. Patients with CNP usually have symptoms of muscle tension accompanied by pain. One previous study has detected that this hyperalgesia was associated with glutamate and prostaglandin E2, which the release of these inflammatory substances and neurotransmitters stimulated the pain receptors to pain [36]. Sjøgaard et al. proposed that the muscle metabolism altered in trapezius myalgia. Lower local blood flow was revealed, and oxygenation of muscle was also slightly insufficient 17 . They suggested that modulation of muscle metabolism may account for the higher lactate, pyruvate and pain responses. Therefore, the causes of intensity of pain might be the biochemical changes of muscles in the neck region. In addition, the intensity of pain could be evaluated by the VAS, which revealed a high reliability in chronic pain 18 . And assessing the intensity of pain in patients with CNP is an essential reference to provide a professional rehabilitation program.
In participants with CNP, the painful region had a stiffer muscle and a higher score of VAS.
These studies about correlation are scientific guidance for physicians to diagnosis and treatment. For example, our previous study has demonstrated that elastic properties of the patellar tendon in athletes with unilateral patellar tendinopathy, and there was a significant correlation between elastic modulus of tendon and functional disability, which it could provide data to estimate whether sportsmen continue their athletic career [11]. A descriptive cross-sectional study about chronic nonspecific neck pain observed that the pressure pain thresholds were associated with NDI in the suboccipital muscle, which indicated a negative correlation (r = -0.288; P < 0.05) 37 . Gonçalves et al. also found a negative correlation between the pressure pain thresholds and NDI in evaluating the upper trapezius in individuals with neck pain. These findings are useful to explore the mechanism of chronic pain 38 . The correlation between intensity of pain from patients and the elastic modulus of upper trapezius in this investigation could be a feasible reference to help rehabilitation therapists diagnose CNP with a more comprehensive assessment.
Chronic neck pain is a common disease in the general population. Findings in this study suggest that the SWE with a high reliability can be used to assess muscle in pathological conditions. And it is expected to be an effective measurement to evaluate quantitatively

Informed consent
Written informed consent was obtained from all subjects invovled in the study. experiment and provided their written informed consent prior to the experiment before study.

Consent for publication
All data published here are under the consent for publication.

Availability of data and materials
The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.    Correlation between intensity of pain and elasticity of the upper trapezius.