Abstract
BACKGROUND:
The persistence of symptoms in patients with chronic neck pain is considered to be associated with variation in the neck muscle structure and associated neuromuscular control. Sling exercise therapy (SET) has been demonstrated to relieve the symptoms of chronic neck pain, whereas it is controversial whether this benefit is correlated to altered neck muscle structure and associated neuromuscular control in the patients.
OBJECTIVE:
To investigate the effect of SET on cervical muscle structure (thickness) and associated neuromuscular control in patients with chronic neck pain.
METHODS:
Twenty-five patients with chronic neck pain were randomly assigned to the SET group (
RESULTS:
At 4 weeks, the SET group had a significant reduction of RMS in both UT and SCM of EMG compared to the control group (
CONCLUSION:
4-week SET was effective in reducing pain and dysfunction in patients with chronic neck pain, which may be related to improved neck muscle thickness and neuromuscular control of the neck.
Introduction
Neck pain is one of the most common musculoskeletal disorders around the world, and neck pain causes patients to have limited daily function [1]. Whilst the majority of patients with neck pain have a satisfactory prognosis for recovery, one third of them still develop chronic neck pain [2]. Chronic neck pain imposes a heavy medical and financial burden on individuals and society, with symptoms of some patients persisting for life [3].
The causative factors of chronic neck pain are complex and most neck pain is unexplained and idiopathic. While current research demonstrated that the persistence of symptoms in patients with chronic neck pain may be related to alterations in the structure of the cervical muscles and the neuromuscular control of the neck [4]. Results from ultrasound studies have shown that patients with chronic neck pain have increased thickness (enhanced stiffness) of the superficial cervical muscles, accompanied by decreased muscle strength of the deep cervical muscles, and that these changes result in abnormal coordination between the deep and superficial cervical muscles [5, 6]. Accurate treatment is based on precise assessment; structures such as muscle thickness can be explored by ultrasound, but direct assessment of the neuromuscular control of the neck is more challenging. The cranio-cervical flexion test (CCFT) provided an option to assess the neuromuscular control of the neck by combining surface electromyography to measure the activity of the superficial cervical muscles to evaluate the interaction between the deep and superficial muscle groups [7]. The available evidence supports that when the CCFT is performed, patients with chronic neck pain have reduced activation of the deep cervical muscles than healthy individuals, accompanied by hyperexcitability of the superficial cervical muscles [8, 9], a finding that is consistent with the observations carried out by Taş et al. through ultrasound [6]. Evidence from ultrasound and CCFT actually illustrated an association between altered cervical muscle structure and altered neuromuscular control in patients with chronic neck pain.
In rehabilitation clinical practice, long-term benefits of interventions for chronic neck pain are extremely difficult to obtain, probably due to the limitations of the location of the deep cervical muscles and most treatments targeting only the superficial cervical muscles [10]. However, relaxation or strengthening of only the superficial cervical muscles only achieves short-term results and is limited to maintaining effective postural correction and symptom relief [11]. The treatment of chronic neck pain should not only focus on the superficial muscles, but should also incorporate neuromuscular control into the core of the treatment, as it is still possible to restore superficial muscle symptoms without changing the coordination and neuromuscular control of the superficial and deep neck muscles. SET is now widely applied in the treatment of chronic musculoskeletal pain and has been demonstrate effective to relieve pain, increase mobility and enhance neck muscle strength in patients with chronic neck pain [12, 13, 14]. Current research confirms that acute SET can alter the thickness of deep neck muscles and neuromuscular control of the neck, but the long-term adaptation of SET to neuromuscular control in patients with chronic neck pain still needs to be investigated [15]. Accordingly, this experiment will investigate the effects of a 4-week SET intervention on clinical symptoms and the muscle structure (thickness) of the neck muscles and neuromuscular control of the neck in patients with chronic neck pain.
Methods
Study design
This 4-week randomized controlled trial was double-blind, two-group, pre-and-post measurement designed. The intervention was performed by a senior physical therapist advanced in SET training, and the outcome variables were measured by other senior physical therapist and sonographers trained in accurate identification and reading. The intervention with the participants was included in the daily routine of the senior physical therapist, who was not involved in this study. The participants in both groups were unaware of each other, and the intervention was carried out in a separate physiotherapy room in the hospital. Participants were recruited and randomly assigned by a research assistant who had no knowledge of this study using simple computer-generated randomization numbers, and the grouping information of the participants was placed in an opaque sealed bottle to ensure that they had no knowledge of the grouping information of others.
Participants
Participants recruitment and eligibility screen for this study was conducted between January 2021 and August 2021 by a senior physiotherapist. The inclusion and exclusion criteria were identified by the same physiotherapist based on previous research [15]. Considering the effects of COVID-19, a detailed check of the subject’s nucleic acid report is required when performing the test and treatment, while the environment is disinfected during the treatment, and both the physical therapist and the patient wear masks properly. The study design and experimental procedures of this study were in accordance with the Declaration of Helsinki, and the study plan was obtained the ethical approval from Shenyang Sport University ethics committee [No, 2020(14)], and was clinically registered (registration number: ChiCTR2200061600). All the participants signed informed consent form prior to participation in this study. Since there was no previous relevant research that could be referred for sample size estimation, the minimum sample size for each group was 12 based on a rule of thumb [16], and the number of participants per group in this study was set at 15 considering a potential attrition rate of 20%.
Inclusion and exclusion criteria
Inclusion criteria: 1) Female patients with chronic neck pain, age range from 40–65 years; 2) The presence of neck and shoulder discomfort, pain, limited movement and other symptoms for more than 6 months; 3) Cervical muscle tension, neck and shoulder pressure points were found by physical examination; 4) Clinicians perform x-ray tests on patients with chronic neck pain, including the following pathologies: changes in physiological curvature, or segmental instability, or intervertebral stenosis, osteophytes, etc. [17].
Exclusion criteria: 1) History of cervical spine surgery, fracture, trauma, infection, tumor, etc.; 2) Other types of cervical spine disease (neurogenic cervical spondylosis, spinal cord cervical spondylosis, vertebral artery cervical spondylosis, sympathetic cervical spondylosis and mixed cervical spondylosis); 3) Combined with severe cardiovascular, pulmonary, hepatic, cerebral, renal, hematological system, severe osteoporosis; 4) Pregnant and lactating women who are not suitable for high-intensity exercise training; 5) People with mental illness or cognitive dysfunction; 6) cervical spine treatment in the past 3 months [17].
Intervention
As shown in Fig. 1, SET was conducted in the sports rehabilitation laboratory, using the Redcord
Visual display of the SET.
Cervical flexor training: The participant was placed in a supine position, with the occipital bone supported by a solid central parting band, the chest and pelvis supported by a wide elastic band, the upper arms crossed in front of the chest, and a soft pad placed under the knee fossa to avoid compensations. The participant was instructed by the physiotherapist to first perform head and neck flexion, then lift the chest, and finally lift the pelvis so that the trunk is in a neutral posture. In this posture, the participant maintained the neck in a neutral position for 2 min, during which the physiotherapist administered a certain frequency of vibration stimulation on the suspension rope. The duration that the participant held the position was recorded, and as the participant’s control ability enhanced, the physiotherapist increased the difficulty of training through shaking the elastic band suspension rope or through extending the time.
Cervical extensor training: The participant was placed in a prone position, supported by a solid center band for forehead, adjusted the height of the center band to relax the cervical spine, maintained normal cervical lordosis within the range of the center band, and placed a soft cushion under the ankle. In this posture, the participant’s neck maintained in a neutral position for 2 minutes, during which the physiotherapist gave a certain frequency of vibration stimulation on the suspension rope. Record the time that the participant maintained this posture. As the participant’s control ability enhanced, the physiotherapist suspended the rope with an elastic band or prolonged the time to increase the difficulty.
Control group
The control group did not participate in any exercise intervention and maintained a normal daily life.
Testing procedures
Visual Analogue Scale (VAS): The validity and reliability of VAS has been demonstrated in the Chinese population [18] and was adapted to measure the pain intensity among participants. A 10-cm VAS ruler has an intensity length of 0 to 10 cm to measure the intensity of pain in the neck area, with extremes defined as “no pain” (0) and “the worst pain imaginable” (10). Participants select a point at VAS that corresponds to the intensity of their pain according to the degree of their competent sensation, and the VAS measurement was repeated three times and the average of the three measurements was taken.
Neck Disability Index (NDI):The Chinese version of the NDI, whose validity and reliability have been demonstrated in the Chinese population, was adapted to assess neck pain and dysfunction. Before filling out the scale, the tester explained to the participant the measurement precautions. During the measurement, the tester explained each option to the participant and took notes accordingly. NDI contains ten self-reported items, including pain (two items), attention (one item), and activities of daily living (seven items). Each item is scored 0-5 according to the degree of cervical spine dysfunction from mild to severe, and the score is proportional to the degree of dysfunction, with 0 indicating no impairment and 5 indicating serious impairment affecting daily life. The interpretation of NDI scores: 0 to 4, no disability; 5 to 14, mild disability; 15 to 24, moderate disability; 25 to 34, severe disability; and greater than 35, complete disability [19].
Musculoskeletal ultrasound testing: Cervical muscle thickness was performed by an experienced sonographer using the GE Logiq e R7 ultrasound with 8–10 linear array transducers (GE Healthcare, Chicago, IL, USA). Ultrasound is a valid and reliable device for measuring the thickness of neck muscle groups (ICC
CCFT: The CCFT was performed by a clinician with more than 15 years of experience. The participant was guided to lie supine with hips and knees flexed, the patient’s neck in a neutral position, and the head and face in a horizontal line, with a soft cushion placed under the patient’s knees to relax the low back muscles and thus avoid tension compensation in the neck. The physician primarily tests the patient complaining of pain on one side, or the most painful if both sides are present. Before the formal test, the participant studied the test procedure to ensure proficiency in the CCFT, while the participant was allowed to rest to avoid fatigue after mastery. The formal test was carried out by performing the standard maneuver of tucking the chin and raising the head about 10 cm above the bed for 10 s, followed by a relaxed rest for 1 min. Afterwards, the airbag of the pressure biofeedback device (Stabilizer, Chattanooga Group Inc., Austin, TX, USA) was placed under the neck, near the occipital bone, ensuring that the head and face were level at this point, using a spare towel if necessary to bring the head to a horizontal position. The airbag was then inflated to 20 mmHg, allowing the airbag to completely fill the subcervical space. After guiding the participant to perform a jaw-retracting nod, the patient was made to look at the instrument meter so that the needle reached each of the five target values (22 mmHg, 24 mmHg, 26 mmHg, 28 mmHg, and 30 mmHg), and each target value was maintained for 10 s and then relaxed for 30 s [4].
Demographic and clinical characteristics of the two groups at baseline
Demographic and clinical characteristics of the two groups at baseline
SET: Sling exercise therapy.
Flow of participants.
CCFT was performed using surface EMG analysis and the test environment was controlled at a temperature of 24
Differences in NDI and VAS between the two groups at baseline
Differences in NDI and VAS between the two groups at baseline
NDI: Neck disability index; VAS: Visual analogue scale; SET: Sling exercise therapy; CI: Confidence interval.
Differences in NDI and VAS between the two groups at baseline
SET: Sling exercise therapy; SCM: Sternocleidomastoid muscle; UT: Trapezius muscle.
All data were analyzed using SPSS 23.0 (IBM Corporation, Armonk, NY, USA), and the normality of the data was tested using the Shapiro-Wilk test (
Results
Participants
For a flow chart of participants, see Fig. 2, 32 subjects were initially recruited for this study and 25 (12 in the intervention group and 13 in the control group) ultimately completed the 4-week intervention and measurement of all outcome variables. Table 1 shows the demographic data of the participants, and there were no significant differences between the two groups at baseline in terms of age, BMI, and course of disease.
Between-group difference
Tables 2 and 3 show the descriptive data of EMG and ultrasound at baseline for the two groups, respectively, and no significant differences were found (
Between-group differences in EMG between the two groups at 4 weeks.
Between-group differences in EMG between the two groups at 4 weeks.
SET: Sling exercise therapy; SCM: Sternocleidomastoid muscle; UT: Upper trapezius.
Between-group differences in EMG between the two groups at 4 weeks.
SET: Sling exercise therapy; SCM: Sternocleidomastoid muscle; UT: Upper trapezius; MVIC: Maximal voluntary isometric contraction.
Table 4 shows the EMG data of both groups at 4 weeks. for SCM, both 22 mmHg, 24 mmHg, 26 mmHg, 28 mmHg and 30 mmHg were significantly lower in the SET group compared to the control group (
Table 5 shows the ultrasound data of both groups at 4 weeks. the SCM data showed a significant reduction in the SET group compared to the control group in both the resting position and the MVIC position (
Between-group differences in ultrasound between the two groups at 4 weeks
SET: Sling exercise therapy; SCM: Sternocleidomastoid muscle; UT: Upper trapezius; MVIC: Maximal voluntary isometric contraction.
Table 6 depicts the pre- and post-group comparisons of the EMG data for both groups. In the control group, there was no significant difference between the pre- and post-intervention (
Table 7 depicts the ultrasound data for both groups, there was no significant difference between the control group in either SCM or UT. the SET group showed a significant reduction in resting level of 0.012 (
Within-group differences in EMG from baseline to 4-weeks intervention
Within-group differences in EMG from baseline to 4-weeks intervention
SET: Sling exercise therapy; SCM: Sternocleidomastoid muscle; UT: Upper trapezius; MVIC: Maximal voluntary isometric contraction.
Within-group differences in ultrasound from baseline to 4-weeks intervention
SET: Sling exercise therapy; SCM: Sternocleidomastoid muscle; UT: Upper trapezius; MVIC: Maximal voluntary isometric contraction.
This study is the first to investigate the effects of SET on neck muscle structure and associated neuromuscular control in patients with chronic neck pain. Previous studies [12, 13, 14] have demonstrated the therapeutic effects of SET in chronic neck pain, including pain alleviation, increased joint mobility, and enhanced neck muscle strength in this population. Whilst potential clinical benefits of SET have been identified, the mechanism by which it mediates improvement in neck pain symptoms is ambiguous. Indeed, changes in neck muscle structure and neuromuscular control are responsible for the persistence of symptoms in patients with neck pain, whereas it is difficult to test the neuromuscular control of the neck directly. Accordingly, this study elected CCFT to detect the activation of superficial cervical muscles to indirectly reflect the neuromuscular control of the neck to assess the effect of SET. Meanwhile, in order to assess the structural changes of the neck muscles before and after the intervention, this study used musculoskeletal ultrasound to detect the thickness of the main cervical muscles. Due to the poor accuracy of the structural description of the deep cervical muscles, superficial cervical muscles were used as the focus of the study. This study actually assessed the possible improvement mechanism of SET by focusing on the structure of the superficial cervical muscles and indirect neuromuscular test.
This study focused on ultrasound images of the superficial neck flexion and extension muscles represented by the superior trapezius and sternocleidomastoid muscles, which are the most active muscles in chronic neck pain, and patients with chronic neck pain usually complain of pain in this area. Taş [6] et al. demonstrated by ultrasound that the superficial neck muscle groups are more rigid (thickness) in patients with chronic neck pain compared to asymptomatic individuals. CCFT also illustrated those higher levels of superficial flexor activity are a sign of reduced activation of deep cervical flexors and that tension in superficial cervical extensors leads to weakness in deep cervical extensors [9, 23]. Ultrasound and CCFT findings suggest altered neuromuscular control in patients with chronic neck pain, which may be closely related to muscle tension between the superficial and deep muscle groups. Janda et al. provided a possible explanation for these phenomena by suggesting that in the presence of pain, the superficial muscles of the neck and back were susceptible to protection, while the deep muscles were susceptible to weakening [24]. Muscle protection may be caused by pain, and when pain persists, a vicious cycle may lead to more muscle protection [25]. We hypothesize that the above phenomenon is related to the functional differences between the superficial and deep cervical muscles. Unlike the superficial cervical muscles that are involved in the regulation of cervical spine motion, the deep cervical muscles mainly involved in maintaining the stability of the cervical spine during prolonged posture and movement [26]. Abnormalities in the function of the deep cervical muscles resulting from prolonged incorrect posture or other causes can therefore lead to compensatory involvement of the superficial cervical muscles in the maintenance of cervical stability, which in the long term can result in tension (hyperactivation) of the superficial cervical muscles and weakness (inhibition) of the deep muscles, ultimately leading to altered neuromuscular control.
This study found that the improvement in pain and clinical symptoms in the SET group may be related to structure of the cervical muscles and the variation of neuromuscular control of the neck. This study found that the recruitment level of SCM and UT decreased with increasing pressure during the CCFT in the SET group after the intervention, whereas this change did not occur in the control group. An explanation for this change has also been provided by many studies [9, 27, 28], which demonstrated that during CCFT, compared to the pain-free group, the neck pain group recruited more SCM and UT with increasing pressure, whereas the pain-free group mobilized more of the deep neck flexors. The ultrasound study also found that the thickness of the superficial cervical muscles also decreased significantly with SET, and our post-intervention results suggest that a potential improvement in neck muscle structure and neuromuscular control occurred in chronic neck pain after the SET. In fact, patients with chronic neck pain who have both muscles seem to have a habit of maintaining a fixed posture for long periods of time, and patients with chronic neck pain experience fatigue of the superficial cervical muscles due to overcompensation, which manifests itself as a decrease in neck muscle endurance in patients with neck pain, and the specific physiological mechanism may be related to a shift in muscle type from slow-twitch type-1 fibres to fast-twitch type-IIB fibres in the above mentioned muscles [29, 30, 31]. SET may have activated the deep layers while avoiding superficial compensations due to fatigue, with eventual symptomatic improvement.
Therefore, in clinical practice, relaxation or strengthening of superficial muscles can only achieve short-term results and is limited to symptomatic relief [11]. Stability training for the deep cervical flexors, on the other hand, can reduce EMG activity in the SCM, anterior trapezius and cephalic grip muscles by increasing the endurance of the deep cervical flexors [32], which is also consistent with the results of our present study. Therefore, based on the above results we hypothesize that SET improving symptoms in patients with chronic neck pain may be based on the following hypothesis: Suspension decreases the compensatory and thus the tension and fatigue of the superficial cervical muscles by activating the deep cervical muscles, which ultimately improves the neuromuscular control of the neck and achieves symptomatic improvement.
Limitations and further recommendations
The first limitation of this study is that the participants were all female, which can reduce the validity of the results. Therefore, the finding obtained cannot be generalized to neck pain patients of all genders. The second limitation is that the age of the participants was concentrated in middle-aged and elderly people, and the obtained results cannot be generalized to neck pain patients of all ages. Third, the sample size was not pre-estimated, but it can be used as a reference for sample size estimation in subsequent large-scaled studies. Finally, this research only conducted the measurement of ultrasonography and surface EMG for one side, thus the difference between both sides was not investigated. Follow-up studies will need to include patients of different genders and ages with chronic neck pain in long-term interventions to further investigate the long-term effects of SET.
Conclusion
The effectiveness of 4-Week SET in reducing pain and dysfunction in patients with chronic neck pain may be related to improved cervical muscle structure and neuromuscular control of the neck.
Ethical considerations
The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by Shenyang Sport University Ethics Committee (No. 2020 [14]).
Funding
This research was funded by a grant from the Basic Scientific Research Projects of Colleges and Universities in Liaoning Province (Grant no. LQN2017ST03 to Yan Gao).
Informed consent
All participants signed an informed consent form prior to enrollment.
Author contributions
ZWY and MZ: Conceptualization, Methodology, Funding acquisition.
ZWY and ZY: Writing-Original draft preparation and Reviewing.
FLZ and YG: Designed the figures.
ZW and JLW: Visualization and Investigation.
All the authors have read and approved the final version of the manuscript and agree with the order of presentation of the authors.
Footnotes
Acknowledgments
None to report.
