https://orcid.org/0000-0003-1689-6190
Figures
Abstract
Background
Differences in cervical neuromuscular function are commonly observed between people with and without chronic neck pain. Exercise may improve cervical neuromuscular function of people with neck pain although the evidence for this has not been systematically reviewed.
Objective
To systematically review the existing evidence on the effect of exercises targeting the neck muscles on neuromuscular function in people with chronic non-specific neck pain.
Methods
This systematic review was conducted based on a registered protocol (CRD42021298831) with searches conducted on the following databases from inception to 21st October 2023: MEDLINE, CINAHL, Web of Science, Scopus, AMED, Google Scholar, Open Grey and Zetoc. Studies of interest were trials investigating neuromuscular adaptations to a program of exercise targeting the neck muscles (>2 weeks) in people with chronic non-specific neck pain. Two reviewers independently screened the studies and performed data extraction, risk of bias assessment, and rated the overall certainty of the evidence (GRADE).
Results
Fourteen articles from 2110 citations were included. There is moderate certainty of evidence that the use of craniocervical flexion training (either in isolation or in combination with resistance training) can induce neural adaptations within the neck muscles. A meta-analysis showed a reduction in sternocleidomastoid muscle activity after neck exercise interventions compared to control interventions.
Citation: Dirito AM, Abichandani D, Jadhakhan F, Falla D (2024) The effects of exercise on neuromuscular function in people with chronic neck pain: A systematic review and meta-analysis. PLoS ONE 19(12): e0315817. https://doi.org/10.1371/journal.pone.0315817
Editor: Sahreen Anwar, Lahore University of Biological and Applied Sciences, PAKISTAN
Received: March 19, 2024; Accepted: December 2, 2024; Published: December 19, 2024
Copyright: © 2024 Dirito et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the manuscript and its Supporting Information files
Funding: The author(s) received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Neck pain is the third leading cause of years lived with disability [1] and is associated with substantial financial and social burden [2]. Neck pain affects all age groups and genders, with the greatest incidence observed for people aged between 45–54 years and for women [3]. Overall, in 2017 the global age-standardized prevalence and incidence rate of neck pain were 3551.1 and 806.6 per 100,000 population respectively [3].
Physical therapy is considered the first line treatment for musculoskeletal disorders with evidence particularly supporting the role of exercise for managing pain, range of motion and disability in people with chronic neck pain [4]. Moreover, some studies emphasize that exercise can be used to enhance neuromuscular function of people with neck pain, potentially leading to better long-term outcomes [5]. This is relevant given the extensive literature documenting changes in neuromuscular function of the neck in people with chronic neck pain [6–8]. This includes increased muscle co-activation [9], changes in coordination between the deep and superficial flexor muscles [10], reduced specificity of neck muscle activity [11] and delayed onset of neck muscles in response to perturbations [12, 13]. People with neck pain also commonly present with reduced neck muscle strength [9, 14] and less endurance [15, 16].
Several systematic reviews have investigated the effect of exercise on neck pain [4, 17, 18]. Overall, these systematic reviews have focused mainly on patient reported outcome measures such as changes in pain intensity, disability, quality of life, global perceived effect, and patient satisfaction. To the best of our knowledge, only one systematic review has investigated the effect of neck exercise on neuromuscular function in people with neck pain [19]. In this review, Blomgren et al. [19] specifically analyzed the effects of craniocervical flexion (CCF) training compared with other forms of training or no exercise on cervical neuromuscular function, in addition to neck muscle size, kinematics, and kinetics. Although this is of relevance, there are many other forms of neck exercise which are relevant to consider when examining the influence of exercise on neuromuscular function, such as resistance training. Thus, in the current systematic review, we consider the effects of all forms of exercise targeting neck muscles and their effect on neuromuscular function in patients with chronic non-specific neck pain. Such knowledge may assist clinicians when planning effective exercise interventions to address neuromuscular function for their patients.
The primary aim of this systematic review is to synthesise the current literature on the effect of exercise targeting the neck muscles performed for at least two weeks on neuromuscular function (e.g., neck muscle strength, endurance, and muscle activity) in people with chronic non-specific neck pain. A secondary objective is to observe if changes in pain intensity and disability are concordant with any physiological changes induced by exercise. This systematic review is based on two hypotheses: 1. exercise may enhance cervical neuromuscular function in people with chronic neck pain and 2. changes in neuromuscular function may explain the positive influence of exercise on pain and disability in people with chronic neck pain.
Methods
Protocol and registration
This systematic review was registered on PROSPERO as protocol No. CRD42021298831 and is reported according to the Preferred Reporting Items for Systematic Review and Meta-Analyses (PRISMA) [20] [S1 File]. The review is based on the updated method guidelines for systematic reviews from the Cochrane back and neck group [21].
Eligibility criteria
Eligibility criteria were based on the PICOS (Population, intervention, comparator, outcome, and study design) framework [22].
Population.
Studies of adults aged ≥ 18 years with chronic non-specific neck pain. Any study where the population was not defined as non-specific neck pain were excluded. This includes studies where participants have neck pain due to pathologies including degenerative diseases, tumors or inflammatory rheumatic disorders and neck pain attributed to an injury (e.g., whiplash). Studies on mechanical neck pain were also excluded as it was not clear from these studies whether a specific pathoanatomical source of pain had been identified.
Intervention.
Any form of exercise targeting the neck region (e.g., motor control, strengthening, endurance) performed for a minimum of 2 weeks without any other additional treatment besides advice or education. This cutoff for training duration was chosen to allow sufficient time for neural adaptations to occur [23]. Trials of rehabilitation or physiotherapy interventions with no specific reference to exercise were excluded.
Comparator.
Comparator studies included no intervention or passive interventions (e.g., manual therapy, education only) or general practitioner management.
Outcome measures.
Outcomes included those measured with electromyography (EMG) such as the amplitude of muscle activity, timing of muscle activity and measures of muscle fatigability. Measures of corticospinal excitability assessed via transcranial magnetic stimulation were also considered. Outcomes which were measures of motor output such as muscle strength, rate of torque development, and endurance were also included. Studies focusing only on muscle morphology e.g., muscle size or fatty tissue, were excluded. Secondary outcomes were self-reported measures of pain intensity and disability.
Study design.
Randomized controlled trials (RCTs), controlled clinical trials and non-randomised studies of exercise interventions.
Exclusion criteria.
Any study not written in English, studies not yet completed and studies that had been published only as a conference abstract or thesis were excluded. Other languages were excluded due to limited resources to translate. No publication time restriction was set for this systematic review.
Information sources
The electronic databases that were searched from inception until the 21st of October 2023 included MEDLINE, CINAHL, Web of Science, Scopus, AMED, Google Scholar, Open Grey and Zetoc.
Search strategy
A comprehensive search for MEDLINE was conducted. The search strategy was generated with Ovid and subsequently the key words of the search strategy were modified using truncation and wildcard searches for the databases listed above [S2 File].
Study selection
All records retrieved in the database search were imported into Endnote (Clarivate Analytics, USA) publication management software. Titles and abstracts were screened, independently by two reviewers (AMD/DA), according to the eligibility criteria. Disagreements were resolved by discussion between the two reviewers. A third reviewer (DF) was available in case of further disagreement [S3 File]. In the second stage of screening, the two reviewers examined the full text [S4 File] to determine their final eligibility [S5 File].
Data extraction process and data items
Two reviewers (AMD and DA) extracted data independently from the articles included in the review; they then compared data extracted and created a single file. Data extracted from the articles included, study details (author, date, location), sample size, participant information, outcome measures, follow up periods (Table 1). Moreover, a description of the intervention was obtained using the Template for Intervention Description and Replication (TIDieR) checklist as guidance (Table 2) [24].
Mean and standard deviation data was extracted for each outcome measure (Table 3). If the mean and standard deviation were not available but this data was presented in figures, we used the WebPlotDigitizer [25] to estimate these data.
Risk of bias assessment
To assess the strength and quality of evidence, two reviewers (AMD and DA) assessed the risk of bias of each study using the Cochrane Collaboration’s risk of bias assessment tool [26]. The Cochrane risk of bias tool assesses bias across 5 domains: Bias arising from the randomization process, bias due to deviations from intended interventions, Bias due to missing outcome data, Bias in measurement of the outcome, bias in selectin of the reported result. The 5 domains are rated as “high,” “low,” or “unclear” risk. Lastly an overall risk of bias has been reported.
Data synthesis
A narrative synthesis was firstly conducted, describing the type of study, variations within interventions, study design, outcome measures, comparability, and comments about the study’s overall quality. Data are reported as “mean ± standard deviation”; p-values have been reported when provided by authors.
A meta-analysis based on EMG data was conducted including 6 of the 14 studies for a total of 9 interventions. This could be achieved for the sternocleidomastoid (SCM) EMG data only. The I-square, heterogeneity measure score, was 0.96 and the CI was -1.715, therefore a meta-analysis could be conducted.
Certainty of evidence
The Grading of Recommendations Assessment, Development and Evaluation (GRADE) [27] method was used to appraise the certainty of the pooled evidence. The overall certainty of evidence for each type of exercise and neuromuscular adaptation was rated using GRADE. The quality of evidence was assessed as “high”, “moderate”, “low” or “very low” by two independent reviewers (AMD/DA).
We rated every article included in this systematic review considering the following criteria described by Guyatt et al. [28]: “risk of bias”, “inconsistency”, “indirectness”, “imprecision” and “publication bias”. Moreover, as suggested by Guyatt et al. [29] we downrated the quality of evidence of methods when the total sample size was low (<24 participants) as this might affect “imprecision”.
Results
Study selection
From 2111 total citations, 47 full texts were assessed for eligibility. The agreement between reviewers was 100% in all stages. Finally, 14 studies are included in the systematic review. The selection process is illustrated via the PRISMA flow diagram (Fig 1). The reasons for the exclusion of articles are reported in depth for each article in S3 and S4 Files. A full list of the 1245 articles screened is provided in S6 File.
Study characteristics
Article information.
Ten articles were RCTs [30–39], one was reported as preliminary RCT [40], and three articles were referred to as randomized trials [5, 41, 42]. The 14 studies were published between 1999 and 2023 and were sourced from different countries: six articles from Asia [30, 33, 34, 37–39], four articles from Europe [31, 32, 35, 36] and four from Australia [5, 40–42].
Participant information.
Table 1 reports the characteristics of the studies. Seven studies did not report a power calculation [30, 33, 35, 36, 39, 40, 42], whereas three based the power calculation on a measure of disability [31, 32, 38], two on subjective reports of pain [34, 37] and two on EMG data [5, 41]. Only three studies included a comparable number of men and women [34, 37, 40], one did not declare the gender of participants [33], whilst the rest of the studies enrolled only women. Regarding the age of participants, 13 articles enrolled patients aged from 25 to 50 years whereas only one article included participants up to 60 years old [39]. Ten articles recruited participants from the general population, and four recruited from the workplace [30, 32, 35, 36].
Exercise interventions.
Table 2 describes the exercises performed in each study including a description of the duration, frequency, and intensity of each exercise. A wide range of interventions were considered: functional postural exercises, shoulder stabilization exercises, strength/endurance exercises, CCF training, mixed training, stretching and Feldenkrais, lateral arm raise, suspension training and global postural re-education, and a program of neck specific exercises. Three studies [5, 41, 42] examined comparable interventions: “endurance/strength training” and “low load CCF training”. Two studies [31, 32] used the same neck specific exercise program described by Jull in 2008 [43].
Comparators.
Regarding the eleven RCTs, three studies [34, 37, 38] offered the control group education regarding ergonomic advice and posture, six [30, 31, 32, 36, 39, 40] did not provide a treatment to the control group, in one [35] they received weekly e-mails about general health education and one [33] provided physical agents.
Outcome measures.
Each study assessed features of neuromuscular function in addition to pain and disability. With respect to the neuromuscular adaptations investigated, seven studies used EMG to assess neck muscle activity during performance of the CCF test (CCFT) or during maximal voluntary contractions (MVC) of the neck muscles. No study used outcomes from transcranial magnetic stimulation. Other outcomes can be seen in Table 3. Regarding patient reported outcomes, neck pain intensity was assessed in eight studies [30, 31, 33, 34, 36, 37, 39, 40] using the Visual Analog Scale (VAS), whereas five [5, 32, 35, 41, 42] used a NRS, and one study [38] used the Neck Pain and Disability Scale (NPAD). Thirteen studies investigated perceived disability: ten studies [5, 30–33, 37, 39, 40–42] utilized the Neck Disability Index (NDI), one [38] the NPAD and one [36] used the Northwick Park pain questionnaire.
Risk of bias.
Two articles showed low risk of bias in all domains [34, 35]. Blinding of participants was not discussed as for the type of studies examined it would have shown 100% high risk. Overall, 11% of bias domains were considered “unclear risk”, whereas 10% were considered “high risk”. Specifically, four articles did not provide a control group [5, 32, 41, 42] (Domain 1: Bias arising from the randomization process), one study showed imbalance between groups [31] (Domain 1), and another one had low sample size [38] (Domain 1). Two articles did not provide clear treatment dose [33, 36] (Domain 2: Bias due to deviations from intended interventions). Four articles [30, 36, 37, 40] did not mention blinding of assessment, so their detection bias (Domain 4: Bias in measurement of the outcome) was reported as unclear. Concerning adherence, two studies [36, 39] had a high risk of bias for incomplete outcome data (Domain 3: Bias due to missing outcome data). One article showed poor methodology that affected randomization, measurement of the outcome and reported result [36] (Domain 1, Domain 4: Bias in measurement of the outcome; and Domain 5: Bias in selection of the reported result). A summary of the risk of bias is presented in Table 4.
Results of individual studies and synthesis of results
An overview of the outcome measures and summary results is reported in Table 1 whereas the means, standard deviations and standardized mean difference for each outcome measure can be found in Table 3. Below we provide a summary of changes in EMG measures as these were common to several studies. All other outcomes are summarized in Table 3.
GRADE has been rated for each study. We then grouped the studies per method to provide a general GRADE score for each treatment type evaluated within this systematic review. A summary of the GRADE rating is presented in Table 5.
Effectiveness and dosage of different exercise interventions
Postural exercises.
Postural exercises were investigated in one trial with low risk of bias [40]. They found less activity of the SCM during performance of the CCFT following training, but no effect on pain and disability. Training was performed every day for two weeks with each session lasting 15–20 minutes. Based on the GRADE assessment, there is a very low level of confidence in the evidence supporting the positive outcomes of neuromuscular adaptations associated with postural exercises.
Resistance exercises (strength/endurance training).
Resistance exercises were investigated in five trials with low risk of bias [5, 30, 38, 41]. Falla 2006 [41] showed decreased EMG amplitude for SCM and AS during isometric neck flexion contractions at 10, 25 and 50% of MVC post training. Falla 2008 [42] found no differences in EMG amplitude of the SCM during the performance of a repetitive upper limb task where patients were asked “to dot pencil marks in three circles in a clockwise direction” [42]. Jull 2009 [5] found no difference in SCM EMG amplitude during performance of the CCFT following a resistance training intervention.
Borisut 2013 [30] found less EMG amplitude during the performance of MVCs in shoulder elevation (upper trapezius, UT), head raising in a prone position (cervical erector spinae, CE) and neck flexion in a supine position (SCM and anterior scalene, AS). Mehri 2020 [38] showed significantly less EMG amplitude and an early activation onset of the SCM and levator scapulae during the performance of MVCs in neck rotation and neck extension, both performed in sitting. All five articles reported positive effects on pain and disability.
These studies provided 8 to 12 weeks of training with three to seven days of training per week. Repetitions were between 12 to 15 and sets from 1 to 3. Based on the GRADE assessment, there is a moderate level of confidence in the evidence supporting these positive outcomes associated with resistance exercises.
CCF training.
CCF training was investigated in six trials with serious risk of bias [5, 30, 33, 41]. The assessment of the risk of bias is influenced by the fact that some articles were not an RCT.
Jull 2009 [5] found a significant decrease of SCM EMG amplitude during performance of the CCFT post training. Falla 2006 [41] showed no difference in EMG amplitude for either the SCM or AS during isometric neck flexion contractions at 10, 25 and 50% of MVC. Falla 2008 [42] found no difference in SCM EMG during the repetitive upper limb task described above; Borisut 2013 [30] found less EMG amplitude for UT, CE, SCM and AS during shoulder elevation (testing UT), head raising in prone position (testing CE) and neck flexion in supine position (testing SCM and AS). Ghaderi 2017 [33] found decreased activation of the SCM and splenius capitis (SCap) and AS during performance of the CCFT. All studies reported positive effects on pain and disability.
These studies provided either a 12-, 8- or 6-week trial with one or two sessions of training per day. Repetitions were up to 15 from levels 22 to 30 mmHg on the CCFT. Based on GRADE assessment, there is a moderate level of confidence in the evidence supporting the positive outcomes associated with CCF training.
CCF training + strength training.
CCF training combined with strength training was investigated in one trial with low risk of bias [30]. Borisut 2013 [30] found less EMG amplitude in UT, CE, SCM and AS during shoulder elevation (testing UT), head raising in prone position (testing CE) and neck flexion in supine position (testing SCM and AS) post training.
This study provided 12-week trial with one session of training per day. Repetitions were up to 15 from levels 22 to 30 mmHg on the CCFT. Based on the GRADE assessment, there is a moderate level of confidence in the evidence supporting the positive outcomes associated with CCF training combined with strength training.
Mixed physiotherapy exercises (Strength + stretching + stabilization exercises).
Mixed physiotherapy exercises were investigated in one trial with very high risk of bias [36]. No changes were observed for SCap or UT EMG or shoulder peak torque during the performance of MVCs in shoulder flexion. The study showed no significant differences in pain and disability following the 16-week trial which consisted of two days of training per week (50min per session). Strength training repetitions were up to 15.
Based on GRADE assessment, there is a very low level of confidence in the evidence supporting the outcomes associated with mixed physiotherapy exercises.
Strength training: Shoulder lateral raise.
Strength training via a shoulder lateral raise was investigated in one article with low risk of bias [35]. This study reported a trend of increased activation of UT and SCap during 90° shoulder abduction, which was statistically significant for the SCap. There was a significant reduction in neck pain intensity.
The training lasted 10 weeks, 5 times per week, increasing the resistance band load every two weeks. Based on the GRADE assessment, there is a moderate level of confidence in the evidence supporting the positive outcomes associated with lateral raise strength training.
Feldenkrais intervention.
Feldenkrais intervention was investigated by one study with very high risk of bias [36]. They showed less activity of UT, SCM and ES during the performance of MVCs in shoulder flexion. Moreover, a significant reduction in pain and disability was recorded. The training lasted 16 weeks with a total of 16 training of 50 minutes.
Based on GRADE assessment, there is a very low level of confidence in the evidence supporting the positive outcomes associated with Feldenkrais intervention.
Cognitive functional therapy + scapular exercises.
Cognitive functional therapy combined with scapular exercises was investigated by one study with low risk of bias [34]. They showed a significant increase of activation in trapezius (upper, lower and middle) and serratus anterior during 90° shoulder abduction. There was a significant reduction in neck pain intensity.
The training was provided for 10 weeks, 3 times per week with progressive load, with participants performing 3 sets of 15 repetitions. It should be noted that the authors provided a cognitive functional therapy based on biomechanical concepts that differs from the one described in literature [44]. Additionally, the recruitment period ended in March 2020, and the study was published in March 2020. There are therefore some concerns about publication bias.
Based on GRADE assessment, there is a low level of confidence in the evidence supporting the positive outcomes associated with cognitive functional therapy combined with scapular exercises.
Scapular exercises.
Scapular exercises were investigated by one article with low risk of bias [34]. They showed a significant increase of activation in trapezius and serratus anterior during 90° shoulder abduction and there was a significant reduction in neck pain intensity.
The training was provided for 10 weeks, 3 times per week with progressive load, 3 sets per 15 repetitions. Based on GRADE assessment, there is a low level of confidence in the evidence supporting the positive outcomes associated with scapular exercises.
Stretching + neck/shoulder strength training.
Stretching combined with neck/shoulder strength training were investigated by one study with low risk of bias [37]. They showed no differences for both CE and UT during 20 minutes of typing. However, neck pain and disability significantly reduced.
The training, using thera-band, was performed at home for no longer than 20 min 4 times per day for 6 weeks. Based on GRADE assessment, there is a very low level of confidence in the evidence supporting the outcomes associated with these exercises.
Suspension exercises.
Suspension exercises for the neck were investigated in one study with low risk of bias [39]. They showed a significant reduction of SCM and UT EMG amplitude during performance of the CCFT. Pain and disability also reduced significantly.
The training was provided for 4 weeks, with 3 sessions per week that last for 20/30 minutes. Based on GRADE assessment, there is a very low level of confidence in the evidence supporting the positive outcomes associated with suspension exercises.
Neck specific exercise program.
A program of neck specific exercises (including CCF training and other low load exercises progressed to higher load resistance training) were investigated in two studies with low risk of bias [31, 32]. Falla 2013 [31] reported less SCM and SCap activity during the performance of isometric contractions for neck flexion, extension and right/left flexion in a sitting position. Both studies reported positive effects on pain and disability. Mendes Fernandes 2023 [32] showed a significant reduction of SCM and AS EMG amplitude during performance of the CCFT. Pain and disability also reduced significantly.
The training was provided for 8 weeks, with 2 sessions per week. Based on GRADE assessment, there is a moderate level of confidence in the evidence supporting the positive outcomes associated with neck specific exercises.
Global postural re-education.
Global postural re-education was investigated in one study with low risk of bias [32]. They showed a significant reduction of SCM and AS EMG during perfor37nce of the CCFT. Pain and disability also reduced significantly.
The training was provided for 8 weeks, with 2 sessions per week. Based on the GRADE assessment, there is a high level of confidence in the evidence supporting the positive outcomes associated with global postural re-education.
Meta-analysis
A meta-analysis could be conducted on SCM EMG amplitude as it was the most common measure investigated. ReviewManager (RevMan) was used to conduct the statistical analysis [26]. Continuous data have been analysed through an inverse variance using a random effect model with 95% confidence interval. The meta-analysis revealed an estimated overall effect size in favour of the decrease of SCM EMG amplitude due to exercise compared to control groups (Fig 2; the data used to generate this figure are provided in S7 File). Moreover, the estimated overall confidence interval does not intersect the “no effect” line, for this reason we can state that the result is statistically significant.
The effect size estimate for the overall outcome is -1.67, with a standard error of 0.73. The Z score is 4.47, indicating statistical significance at a two-tailed significance level < 0.00001. The 95% confidence interval ranges from -2.40 to -0.94, suggesting a statistically significant effect. Overall, this supports a reduction in SCM EMG amplitude in response to training.
Discussion
This is the first systematic review that comprehensively investigates the effect of exercise on neuromuscular adaptations within the neck muscles in people with chronic non-specific neck pain. Seventeen different exercise approaches from fourteen studies were assessed. Analysis of information was limited by low sample size, differences in exercise dosage, different duration of exercise, and a lack of data about dosage and description of the exercises performed. Thus, a narrative synthesis of the data was carried out for the most part apart from a meta-analysis on changes in SCM EMG amplitude after exercise which shows a reduction of SCM activity after exercise in people with chronic non-specific neck pain. Although this systematic review considered measures obtained with transcranial magnetic stimulation as an outcome measure, none of the 14 articles included used this outcome measure.
All RCTs but two [34, 35] assessed SCM activity via EMG, therefore we were able to synthesize the results from these RCTs [30, 31, 33, 38–40] with a meta-analysis. The overall effect size shows a decrease in SCM EMG activation in response to exercise. Five articles specifically assessed neck muscle activity via EMG as participants performed the CCFT [5, 32, 33, 39, 40] while the other articles examined different tasks. Overall, the results support a reduction of superficial muscle activity (SCM, AS, SCap and UT) during the CCFT following a period of exercise [32, 33, 39, 40]. The study by Jull 2009 [5] was the only article that assessed the deep cervical flexors (longus capitis and longus colli) during performance of the CCFT following exercise and demonstrated an increase in EMG amplitude of the deep cervical flexors during performance of the CCFT following CCF training. The same study also reported no change for the same outcome after neck strength training.
Results varied for other tasks but what became evident from the results is that the type of adaptation closely reflects the type of training performed. For example, Jull 2009 [5] reported improved neuromuscular control of the deep and superficial neck flexors following 6-weeks of CCF training but not following strength training of the neck flexors, even though neck pain intensity reduced by a comparable amount in both groups. Likewise, Falla 2006 [41] reported a reduction of EMG amplitude for the SCM and AS during isometric neck flexion contractions at 10, 25 and 50% of MVC following a resistance training program for the neck flexors yet there were no changes on this task for those that performed low-load CCF training. Furthermore, Falla 2008 [42] found no differences in the EMG amplitude of neck muscles during an upper limb task after either a neck endurance-strength training program or CCF training and Ma 2011 [37] found no differences in the activity of neck muscles during an upper limb task after neck muscle strength training. A further example is the study by Jull 2009 [5] which reported no statistically significant difference in the relative latency of neck muscle activity during rapid arm movements (flexion and extension) following either CCF training or resistance training. However, there were some situations where changes in neuromuscular function did not relate specifically to the type of training performed. For example, Mehri 2020 [38] showed a faster onset of superficial neck muscles (UT, SCM and ES) during an anterior-posterior perturbations following a program of progressive resistance exercises, while Ghaderi 2017 [33] showed a faster onset of SCM AS and SCap during rapid arm movements following CCF training. Thus, the majority of studies from this systematic review suggest that changes in EMG measures (muscle and task) closely match the type of exercise performed although, there were exceptions.
In the current systematic review, we considered studies with a treatment duration of at least 2 weeks. Two studies, Beer 2012 [40] and Yan 2022 [39], provided 2- and 4-weeks of training respectively, whereas Lundblad 1999 [36] used a program of 16 weeks, and the other studies used an exercise program which ranged between 6 to 12 weeks. Both Beer 2012 [40] and Yan 2022 [39] showed that 2 weeks of neck flexor and extensor training are sufficient to decrease SCM and UT EMG during performance of the CCFT. Thus, it appears that cervical neuromuscular adaptations occur rapidly with training, and this is line with an abundance of research reporting early neural adaptations to training [45]. Nevertheless, the advantages of longer periods of training versus shorter durations remain to be investigated.
All articles in this systematic review demonstrated a positive improvement in pain and disability following training, except for the studies by Lundblad 1999 [36] and Beer 2012 [40]. Lundblad 1999 [36] showed no changes in disability in both groups (Feldenkrais or physiotherapy) after 16-weeks of training. However, it should be noted that there were several limitations to this study as detailed in the risk of bias assessment, but additionally, the choice of the outcome measure might have potentially impacted the results. While all other articles used the NDI or NPAD, Lundblad 1999 [36] assessed disability with the Nordic Council of Ministers questionnaire that seems to have suffered floor effects in this situation, since the baseline data were already low.
The study by Beer 2012 [40] was the only study that reported changes in EMG measures of neck muscle activity, but no improvement in either pain or disability. However, the study by Beer 2012 [40] was the one with only a 2-week training program, and as such it was possibly insufficient to result in significant pain relief despite early neural adaptations to training. Further studies are necessary to understand the temporal development of neuromuscular adaptations to training and changes in patient symptoms.
Strengths and limitations
This review employed rigorous methodology and was conducted according to a published protocol on PROSPERO (CRD42021298831) and reported in line with PRISMA guidance. The quality of the included studies was reduced due to low sample size, differences in exercise dosage, different duration of exercise, and a lack of information on the actual exercises. Moreover, we encountered some difficulties in comparing EMG data between studies given the range of tasks assessed (e.g. CCFT, typing task, shoulder MVC, upper limb task). A further limitation of this systematic review is the language restrictions which were imposed on our searches.
Conclusions
There is moderate certainty of evidence which supports the use of CCF training (in isolation or in combination resistance training) in patients with chronic non-specific neck pain to induce neural adaptations within the neck muscles. The majority of the results support the notion that neural adaptations to training are specific to the task trained. Further RCTs are needed to evaluate neuromuscular adaptations within deeper neck muscles in response to both CCF training and strength training.
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