Effectiveness of the scapula mobilization technique on the neural mechanosensitivity of the upper limb neural test 1 in individuals with mechanical cervicalgia. A randomized controlled trial

Effectiveness of the scapula mobilization technique on the neural mechanosensitivity of the upper limb neural test 1 in individuals with mechanical cervicalgia. A randomized controlled trial Carlos Heredia Macias a,* , Javier Ramos Ortega b , Francisco Javier Serrano- S a ´ nchez a , Juan Antonio Díaz-Mancha a , Lourdes Fern a ´ ndez Seguín a , Jaime Caba n ˜ es-García a a Physiotherapy Department, Spain b Podiatry Department, University of Sevilla, Spain A R T I C L E I N F O Handling Editor: Dr Jerrilyn Cambron Keywords: Neck pain Median nerve Neuralgia Nerve compression syndromes and dynamic stretching A B S T R A C T Objective: to observe whether the mobilization of the scapula improves the mechanosensitivity of the median nerve in patients with cervicalgia. Localized cervical pain caused by compression of a nerve root without presenting irradiated features along the nerve path is diagnosed as cervicalgia. Muscles around the scapula can be directly responsible of this compression. Methods: 60 adults diagnosed with cervicalgia and with a positive upper limb neural test 1(ULNT1) were recruited. Participants in the experimental group received a scapula mobilization technique. Participants in the control group, with electrodes on both sides of the neck and connected to turned off analgesic current device, received an abductionadduction mobilization of the calcaneus in the lower limb contralateral to the painful area. The variables measured were pain, goniometry of elbow extension in movement for the median neurodynamic test (ULNT1) and hand grip strength. Results: Results showed that the increase in strength (p = 0.01) and elbow extension movement (p = 0.01) and the decrease in pain (p < 0.01) from the intervention group showed significant changes compared to the changes from control group. Conclusion: Scapula mobilization technique in subjects presenting with cervicalgia and a positive ULNT1 significantly appears to help improve the neural mechanosensitivity of the median nerve and pain. Introduction Mechanical cervicalgia is a very frequent clinical condition that can be considered a pluripathology since it covers somatic, functional, psychological and social aspects (Duyur et al., 2009; Pinto-Meza et al., 2006). Mechanical neck pain (MNP) is characterized by non-specific discomfort at the cervicothoracic junction that may or may not radiate to the upper extremity. There are myofascial expansions (ME) where the deep fascia (DF) joins the various muscles of the upper quarter region (UQR), which may result in cervicobrachial discomfort and nociceptive pain (Raja et al., 2023) It is suffered by high percentage of the general population during some period of their life and constitutes one of the most frequent reasons for absence from work and the main cause of permanent absence from work (Albert and Bosca, 2008; Hogg-Johnson et al., 2009; Steenstra et al., 2006). Many of these patients are diagnosed with nonspecific neck pain (Guzman and Hurwitz EL, 2008), a diagnosis that does not indicate a clear structure as a cause of pain and therefore favors the patient being treated with multiple therapeutic treatments (Koes et al., 1992; Vonk et al., 2004). Given the chronicity of the symptoms in these patients, it is important that the responsibility for the mechanosensitivity of the nervous tissue in this process is delimited (Barry and Jenner, 1995). Because over the last decade the nervous system has been given greater clinical importance as a source of musculoskeletal problems in patients with chronic mechanical cervicalgia (Brix et al., 2013), neurodynamic provocation tests have been developed, such as the Upper Limb Neural - Test 1” (ULNT1). The ULNT1 consists of a series of movements constructed to stress various parts of the nervous system and is regarded to be capable of detecting increased nerve mechanosensitivity. Furthermore, musculoskeletal physiotherapists evaluate ULNT1 (median nerve) to discover changes in mechanosensitivity in the neural system, hence measuring function gain for patients (Lin et al., 2022). Regarding the path of the median nerve, it should be noted that the subscapular and pectoralis minor muscles have direct insertion of the scapula, hence it is necessary to demonstrate the importance of the scapula dysfunctions in cervicalgia with a neurogenic component given the intimate topographic relationship between the pectoralis minor and the brachial plexus (Frank and Netter, 2019). It will thus be possible to check the relationships that the nervous tissue has with cervical pain diagnosed as nonspecific. In the scapulothoracic joint, there is no bone congruence between the scapula and the thorax, which explains the three-dimensional nature of the biomechanics at this level. Therefore, the different possible movements, e.g., protraction, retraction, elevation, depression, anteroposterior tilt, and internal-external and upward-downward, are usually combined (Paine and Voight, 2013). Additionally, the acromioclavicular joint is responsible for the initial 30◦ of shoulder abduction and 60◦ of shoulder flexion, with no direct relationship with the humerus. From this point on, every 2◦ of movement at the glenohumeral joint corresponds to 1◦ at the scapulothoracic joint (Peat, 1986). This scapular mobility can be highly influenced by retractions of the soft tissue, hence mobilization of the scapula during the early stages of rehabilitation is recommended after surgery of the shoulder complex (Paolucci et al., 2021). It has also been used in addition to corrective exercise and taping for neck pain and scapular dyskinesia (Alshami and AlSadiq, 2021). Our hypothesis is that scapula mobilization in these patients, compared with the placebo, decreases pain and increases the elbow extension range of movement and the hand grip strength. Therefore, the present study aimed to evaluate the effects of scapula mobilization, compared with a sham placebo, on pain intensity, grip strength, and elbow extension range of movement during the ULNT1, in individuals with mechanical cervicalgia and with a positive response to the ULNT1. Method Design A single-blinded randomized-controlled clinical trial was carried out. Participants Subjects diagnosed with mechanical cervicalgia and with a positive ULNT1, who volunteered to participate, were consecutively recruited at our Physiotherapy and Osteopathy Center. Participants were diagnosed by a specialist physician after imaging tests (the main tests performed were radiography and magnetic resonance imaging) were conducted and no anatomical source of pain was identified. The exclusion criteria were as follows: any musculoskeletal problems that prevented to conduct the ULNT1, congenital malformations of the cervical spine and/ or upper limb, previous spinal surgery, previously diagnosed neurological pathologies such as diabetic polyneuritis or others as facet joint dysfunction, spurling and/or distraction test, TOS, nerve compression at the elbow and/or wrist. Research design was approved by the Research Ethics Committee of the Virgen del Rocío and Virgen Macarena Hospital of Sevilla (promoter code: JACAGA1 internal code: 0399-N-16). All participants signed their informed consent to participate in the study. The protocol was prospectively registered in clinicaltrials.gov with code NCT04168476. The study was conducted between November 2019 and October 2020. Randomization and blinding A senior physiotherapist with more than 18 years of manual therapy experience conducted the ULNT1. Those with a pain-evoked response during the test were randomly distributed into the study groups. Positive cases, that is, those where pain appeared during the test, were randomized. The subjects were randomly divided by putting in 30 ballots that read A (intervention group) and 30 ballots that read B (control group) in an envelope, where the subject reached in and pulled out a ballot at random. Inclusion in each group was only known by him. This same therapist performed the treatment maneuvers on both the control group and the intervention group. Post-treatment evaluations were carried out by another physical therapist who was blinded to which participants belonged to each group. In summary there were 4 physiotherapists involved, one physiotherapist who did the screening and assessments, a second who did the treatment, the third one who performed the randomization with microsoft excel and the fourth who guarded the randomized envelopes. Study protocol Clinical and demographic data were initially collected. After that, participants underwent the ULNT1, and those with a positive response to the test were randomly distributed into one of the study groups. An independent researcher used Microsoft Excel’s randomization function to complete the randomization schedule for treatment order, taking into consideration a 1:1 ratio distribution of participants in the study groups, the Intervention Group and the Control Group. An external assistant, not involved in the clinical trial, safeguarded the randomization sequence, and sealed opaque envelopes were used to conceal the treatment order allocation. For the ULNT1 the patient was placed supine on the stretcher and without a pillow, with the arms along the trunk and the shoulders parallel to the upper edge of the stretcher (Kay et al., 2015; Mathiowetz et al., 1984). The therapist on the side of the arm evaluated, looking at the patient’s head, fixed the patient’s shoulder with his/her medial hand without applying pressure when fixing it against the stretcher. The lateral hand made contact with the palm of the patient’s hand and performed a 110◦ abduction and glenohumeral external rotation, elbow flexion, forearm supination and finger extension (Fig. 1). From this position, the therapist performed the elbow extension. It is important that, during the movement, the patient would not have performed a glenohumeral induction; therefore, the arm would rest on the assessor’s medial thigh (Fig. 2). The test ended when, during the extension movement, tension and pain were triggered in the patient; the angle where pain symptoms began to appear was measured goniometrically. Once the subjects were selected, the first assessment of pain, prehensile strength and goniometry in elbow extension was performed until Fig. 1. Fig. 2. pain onset during the ULNT1. The intervention was performed in both study groups by a physiotherapist with more than 10 years of clinical experience. The second evaluation was carried out immediately after intervention by a different physiotherapist. From the time the patient is assessed by the first assessor to the time the patient is assessed after the intervention, the duration of each collection was 45 min. Measurements Degrees of elbow extension for the ULNT1. The ULNT1 procedure was performed until the patient described to the assessor that his/her pain was beginning to appear; at that point, the assessor stopped the test and measured the elbow degrees with a goniometer with a European Community marking. The amplitude of the elbow movement was assessed by considering a series of anatomical references which, for the inner side, are as follows: cubital styloid processes for the distal goniometer arm, medial epicondyle of the humerus for the goniometer axis, and humeral diaphysis for the proximal arm (Norkin and White, 2006). Pain was measured through the VAS (visual analogic scale). The participant was asked to report the neck pain intensity in a 0 to 10 scale, where 0 denoted “absence of pain” and 10 indicated “the maximum tolerable pain”. Prehensile hand strength was measured with a Baseline Hydraulic Hand Dynamometer® (Fabrication Enterprises Inc, Irvington, NY). To make the measurement, the subject was sitting, shoulder adducted and in neutral rotation, 90◦ elbow flexion, neutral forearm position, wrist in slight dorsal flexion (always between 0◦ and 30◦) and a cubital deviation of between 0◦ and 15◦. In this position the subject energetically grips the dynamometer to the maximum extent they can. Three measurements were taken and the mean value calculated (Mathiowetz et al., 1985, 1986). VAS, Prehensile hand strength and goniometry in elbow are a valid assessment tools with a high inter-observer reliability (Gharib et al., 2019; Paulis et al., 2011; Swanson et al., 2019). Interventions After the first evaluation, the intervention group received the scapula mobilization technique described by Travell and Simons (Simons et al., 1999). The patient remained in lateral decubitus, with the affected side on top. The researcher stood in front of him, passed his cephalic hand over the patient’s shoulder to access the top of the medial edge of the scapula, while, with the other hand, he reached the bottom of that edge, passing under the humerus. From this point on mobilizations were performed in scapula elevation-depression, scapula external-internal rotation and scapula abduction. To standardize the intervention and make it reproducible in each patient, 10 mobilizations were performed in each of those three movements and in the mentioned order and after the technique they were reassessed. The control group subjects received a mobilization in abduction-adduction of the calcaneus of the opposite leg to the measured side. In addition, 5 × 5 cm electrodes were placed on both sides of the neck, connected to turned off analgesic current device. Statistical analysis The minimum sample size required was calculated using the free distribution software Granmo 7.12. For this, a pilot study was used based on mean differences in elbow goniometry (control group mean 124.8; intervention group mean 149.73). Thus, the following parameters were considered to calculate the size: estimation of independent group means, two-tail hypothesis, type I error - 0.05, type II error β = 0.20, standard deviation of 25.7% in elbow goniometry, minimum difference to be detected of 24.9◦ between the intervention group and the control group, the expected maximum loss proportion of 20%. Under these parameters a minimum sample of 21 individuals in each group was recommended to us. This study eventually included 30 individuals in each group. Statistical analysis was performed using the PASW Advance Statistics (version 23.0; SPSS, Inc, Chicago, IL). Data were reported as mean and standard deviation. The normality of the variables was analyzed using the Kolmogorov-Smirnov test (p < 0.05). The Mann- Whitney U test were used to study whether there were differences for each study situation. To calculate the effect size the Cohen’s D test was used. An alpha of 0.05 was determined as the significance level. Results A total of 60 adults (33 females and 27 males) with a mean age of 46.4 ± 3.23 years were recruited (Fig. 3). None of participants reported minor or severe adverse events during the study protocol. Table 1 lists the clinical and demographic features of participants, with no differences in the comparison between groups in any of the study variables at baseline (all, p > 0.05). Table 2 includes the analysis between groups of the mean changes after intervention in selfreported pain, range of movement and grip strength. These differences were statistically significant for all outcome measures (all p < 0.05), with moderate to high and very high effect sizes for strength, pain, and range of movement, respectively. Discussion The aim of this study was evaluating the effects of the mobilization of the scapula in subjects with mechanical cervicalgia and positive ULNT1. We found statistically significant results for the changes in the three variables studied. The changes in the goniometric measurement in our study were a significant difference (p = 0.01) and a very important effect size (1.86). There are few studies in which the neurodynamic test is used as a maneuver to provoke pain as well as evaluation of its development after the experimental technique. Coppietiers et al. (Coppieters et al., 2003) Fig. 3. Table 1 Descriptive statistics of the variables. VAS: visual analogic scalenew VARIABLES CONTROL INTERVENTIO N P SEX, M/F 15/15 12/18 0.436 EXPLORED MEMBER, L/R 16/14 10/20 0.118 AGE, years 48.87 ± 13,56 43.9 ± 11.36 0.425 STRENGTH PRE, kg 28.93 ± 10.86 29.93 ± 8.87 0.35 VAS PRE, scale 0-10 4.90 ± 2.14 4.55 ± 1.76 0.52 GONIOMETRY PRE, degrees 126.23 ± 21.21 128.90 ± 19.33 0.84 Table 2 Difference between post values and pre values of the variables and comparison between groups. PRE/POST CONTROL INTERVENTI ON P EFFECT SIZE CHANGE —1.9 ± 6,04 16.66 ± 9.47 0.01 1.86 GONIOMETRY CHANGE VAS —0.55 ± —1.73 ± 1.79 <0.001 0.7 1.57 CHANGE —0.57 ± 1.05 ± 2.65 0.01 0.19 STRENGTH 2.06 compared the effect of a cervical lateral slide as neuromeningeal dynamization, with the effect of an ultrasound therapy. In the lateral slide group, the results showed significant improvements (p < 0.003) in the increase in the elbow extension from 137.3◦ to 156.7◦, in the 43.4% reduction in the symptom distribution area and in the reduction in pain intensity from 7.3 to 5.8. For the ultrasound group, there were no significant improvements (p < 0.521). In our study we achieved an improvement in pre- and post-goniometry of 16.66◦, on mean, which are similar figures to the Coppieters et al. study. Like Coppieters, we assessed an immediate effect and the effectiveness of a manual therapy technique, the aim of which is to produce a neuromeningeal slide that promotes the function of the neck and upper limb, which can produce improvement in all the assessed parameters. Both Coppieters et al. and our findings demonstrate that the presence of sensory responses such as pain provocation and movement limitation in the ULNT, even if present in asymptomatic subjects, does not put at risk the test’s discriminatory capacity in the event of a pathology. As regards the scapula mobilization technique used in our study, we could say that it could improve the goniometry on the basis of two hypotheses: on the one hand, because it constitutes a neural mobilization, and on the other, because manual therapy reduces muscle tone (Hammill et al., 1996). By this mechanism, the scapula mobilization technique could reduce the tone of the muscles innervated by the brachial plexus nerves (Frank and Netter, 2019). In our study we found a significant difference in the registered changes in VAS comparing between groups (p < 0.001) and a medium effect size (0.7). There are randomized controlled trials that demonstrate that the use of placebo treatments can decrease neuropathic pain without hyperalgesic effects (Vase et al., 2016). Other studies conclude that suggestive actions (i.e, the fact that the patient goes to a physiotherapy clinic and is treated, as in the present study) and administration of placebos can develop physiological responses (Haga et al., 2009). Similarly, the use of placebo may induce expectations of analgesia and help to recall previous experiences to relieve pain (Colloca et al., 2013). However, in intervention group we have made a technique seeking a relaxing effect on the structures that are inserted in the scapula and we have obtained a significant decrease of pain compared to the decrease in the control group. Savolainen et al. (2004) shows more significant pain reduction in a group where spinal manipulation is performed than in another group where an active exercise program is begun. This is also demonstrated by Fernandez de las Pen˜as et al. (Ferna´ndez de las Pen˜as et al., 2011) in subjects with neck pain in whiplash pathology (VAS), specifically after the first 4 sessions, with a 40% reduction in EVA (p = 0.003). In these studies, chest manipulation was compared with another type of intervention and over several weeks both groups of subjects improved. We must add that physical exercise as a treatment for chronic non-specific neck pain was shown to be a therapeutic tool with good clinical effectiveness (Hammill et al., 1996; Kay et al., 2015) In our study prehensile force increased significantly after mobilization of the scapula. Buttler (David S. Butler, 2002). points out that neural mobilization can improve muscle activity by improving the circulation of axoplasmic flow, which favors the health of muscle tissue innervated by the mobilized structure. This point may explain the increase in isometric strength of the muscle after neural mobilization. Likewise, Flauzino et al. (Flauzino Machado et al., 2015) assessed the influence of mobilization of the median, radial and ulnar nerves on prehensile force, observing significant changes (p < 0.05) post-intervention in the median and radial nerves; these changes remained for the following 24–48 h only in the median mobilization group. Unfortunately, the absence of a control group in this study limits interpretation regarding its clinical efficacy. It is important to note that in these studies the neurodynamic test has been carried out as a neural dynamization maneuver, that is, as a treatment and not as an evaluation tool as it is in our case. Childs et al. in their guide for the clinical practice of neck pain (Childs et al., 2008), recognize that the anterior, middle and posterior scalene muscles, upper trapezius, elevator scapulae, pectoralis minor and pectoralis major, are key to proper cervical functioning such that the mobilization of the scapula would influence several of these muscles and may improve the mechanosensitivity of the brachial plexus. Many of the studies we commented on in the discussion have limitations, such as no control group or using several physical therapy techniques that led to repeated interventions over several weeks. In our view, it is preferable to use a single technique in order to quantify the changes in the intervention group and to use a placebo technique in the control group, thus avoiding multiple interferences over the course of the study. In this work we did not seek to assess the long term effects of the changes obtained with the scapular mobilization. We consider it useful to be able to observe the effect of a therapeutic technique used in daily clinical practice, without possible interference caused by the patient’s change of habits over subsequent days or other circumstances, and thus obtain greater scientific evidence that scapula mobilization immediately improves the neural mechanosensitivity of the brachial plexus, increases prehensile strength and decreases pain in patients with mechanical cervicalgia. A study with different interventions over several weeks can lead to changes caused by other factors. Moreover, in mechanical cervicalgia as a non-specific neck pain, the etiological causes on which to work to alleviate the ailments of the subject are unknown. That is why seeking to test the effect of the technique within a population in which the cause of said problem is not clearly identified can constitute a bias in the results obtained over time. Limitations Some limitations should be acknowledged. Based on previous clinical experience, the treatment protocol included 10 repetitions of different scapular movements. Further research should investigate whether different approaches with a more progressive or demanding number of sets and repetitions could achieve similar results. Our findings are also limited to a rather small sample size and the assessment in an immediate fashion. Future lines of research are needed to investigate if the effects can be sustained over time and may be similar in patients with different neck-shoulder musculoskeletal conditions, e.g., cervicobrachial neuralgia. Likewise, the use of multidimensional tools to assess pain could help to better understanding the clinical effect of the intervention. Conclusion Mobilization of the scapula helps to immediately improve mechanosensitivity of the median nerve, elbow extension, self-reported neck pain, and grip strength in adults with mechanical cervicalgia. Further research should investigate the medium and long-term effects of the proposed protocol. CRediT authorship contribution statement Carlos Heredia Macias: Methodology. Javier Ramos Ortega: Writing – review & editing. Francisco Javier Serrano-Sa ´ nchez: Investigation, Conceptualization. Juan Antonio Díaz- Mancha: Writing – original draft, Supervision. Lourdes Ferna ´ ndez Seguín: Data curation, Conceptualization. Jaime Caban ˜ es-García: Project administration, Formal analysis. Declaration of competing interest