Functional reorganization of cervical flexor activity because of induced muscle pain evaluated by muscle functional magnetic resonance imaging.
From: Man Ther. 2011 Mar 22. [Epub ahead of print]
Neck pain is a common and disabling health problem with up to 70% of individuals experiencing an episode in their lifetime. The prevalence of neck pain, and as a consequence the social burden of this problem, have been increasing during the past several years. Although all cervical muscles contribute to the support of the cervical spine, the deep cervical flexor muscles (longus colli and longus capitis) have particularly demonstrated changes in the morphology and neuromotor control in patients with painful neck pain disorders. Such changes include increased fatty infiltrates in the flexors of subjects with whiplash associated disorders as well as changes in the timing and activity levels of the flexors in neck pain patients.
The function of these muscles in healthy and clinical populations has mainly been investigated by use of a craniocervical flexion task, as this movement specifically targets the deep cervical flexors, with minimal activation of the superficial cervical flexor muscles such as the sternocleidomastoid muscles. Several studies have demonstrated that individuals with chronic neck pain exhibit increased activity in the sternocleidomastoid during the craniocervical flexion task which was assumed to be a compensation for reduced deep cervical flexor activation. Only Falla et al. (2004) has directly recorded a reduction in activity of the deep cervical flexors in neck pain patients by use of a nasopharyngeal electromyography (EMG) technique capable of reaching these deep-lying muscles. However, this technique is quite invasive, does not allow for the differentiation of signals between the longus colli and longus capitis muscles and is vulnerable to muscle cross-talk, which highlights the need for alternative techniques.
There are a number of hypotheses as to why differential muscle recruitment in patients with neck pain exists. The current evidence suggests that pain may immediately induce an altered control strategy which in turn may contribute to muscle overload or disuse and additional adaptations at the muscle level in the long term. Jull et al. (2008) recently stated that it is assumed, from clinical observations, that deep cervical flexors demonstrate changes very early following the onset of pain or injury. This however needs to be substantiated. One method of further investigating the temporal relationship between the onset of pain and changes in neuromuscular control is the use of experimental pain paradigms. Experimental pain methods permit investigation of cause–effect relationships between muscle pain and muscle function during a specific task. However, to date no study has investigated if pain has an immediate effect on activity of the deep cervical flexor muscles, partly due to the difficulty of direct quantification of this muscle group.
A method that is gaining popularity in evaluating deep spinal muscle function is muscle functional magnetic resonance imaging. This method is non-invasive and permits observation of the differential activation of deep and superficial cervical flexor muscle layers. This level of differentiation is essential to examine separately the activity of the longus colli and longus capitis muscles, which based on their individual anatomical configurations are likely to differ in their anatomical action. The technique is based on an acute enhancement of the T2 relaxation time (T2) of muscle water following activation and provides information regarding the pattern and the intensity of the muscle activity.
The purpose of this study is to investigate the effect of experimental muscle pain on the activity of the cervical flexors (longus colli, longus capitis and sternocleidomastoid) by use of mfunctional magnetic resonance imaging during the performance of a craniocervical flexion task.
At least one week prior to the test day, subjects were instructed in the action of craniocervical flexion. In supine lying, subjects first carefully practiced the craniocervical flexion action, performing a gentle nodding action of the head without lifting the head off the supporting surface until full craniocervical flexion range of motion was reached. Once the correct movement pattern was achieved, a pressure cuff (Stabilizer) was placed suboccipitally behind the subject’s cervical spine and inflated to a stable pressure of 20 mmHg. This pressure cuff monitors the progressive flattening of the cervical lordosis that occurs with the incremental stages of this craniocervical flexion task (progressive craniocervical flexion effort toward inner range), which is subsequently registered as an increase pressure reading. Subjects practiced progressive targeting of five incremental levels (increment, 2 mmHg) between 22 and 30 mm Hg by maintaining a steady pressure at each target (mmHg) for 10 s. The pressure level that the subject could achieve and hold in a steady manner for 10 × 10 s with the sternocleidomastoid relaxed and without lifting the head off, the surface was determined. At the test day, subjects were asked to accurately maintain the predetermined pressure level and to execute a 1 min isometric hold. The exercise was performed three times with 15 s of rest between the sets. A correct movement pattern was guided by visual feedback of the pressure cuff and controlled by an examiner. Rate of perceived exertion (RPE) was reported after each exercise bout, both in the pain and non-pain conditions.
This study has confirmed that pain has an immediate impact on the activity levels of the deep cervical flexor muscles during the performance of a craniocervical flexion task. This is a demonstration of a functional reorganization of these muscles in the presence of pain similar to that shown in clinical populations.
In the non-painful state the sternocleidomastoid showed a significantly lower T2 shift than longus colli and longus capitis during the craniocervical flexion task. This is in accordance with previous EMG-studies which demonstrated that the craniocervical flexion method is more specific to the anatomical action of the deep cervical flexor muscles, and less specific to the function of the superficial cervical flexors. An added value of using functional magnetic resonance imaging is the possibility of distinguishing between the actions of the longus colli and the longus capitis, which is not possible with EMG. Cagnie et al. (2008) investigated muscle activation during different cervical flexion exercises and found that the longus capitis displayed a significantly higher T2 shift during the craniocervical flexion task compared to the longus colli and the sternocleidomastoid. One of limitations of this study was that the longus capitis was evaluated at the C0–C1 level, whereas the longus colli and sternocleidomastoid were investigated at the C5–C6 level. The current results confirm the assumption that craniocervical flexion is the primary action of the longus capitis together with the superior portion of the longus colli. This is in accordance with the study of Cagnie et al. (2010) who recently demonstrated the largest increases in cross-sectional area at the C0–C1 level for the longus capitis (11.1%) and at the C2–C3 level for the longus colli (17.4%) during the performance of craniocervical flexion.
In the presence of the experimental pain a decrease in T2 shift was observed for both the longus colli and longus capitis muscles. This reduction was bilateral and multilevel indicating a generalized motor response. The sternocleidomastoid did not demonstrate a change in T2 shift between the pain and non-pain conditions, except for the left sternocleidomastoid at the C6–C7 level, which demonstrated an increase in T2 shift following injection of hypertonic saline.
Until now, it was hypothesized, but not substantiated, that pain induces an immediate inhibition of the deep cervical flexors. This study is the first to investigate changes in the deep cervical flexors by use of an experimental pain paradigm. It is consistent with the observations in a clinical population of a rapid change in neuromuscular control associated with the onset of neck pain. It is also consistent with previous studies investigating the activity of other cervical muscles (trapezius, splenius capitis and sternomastoid muscle) in response to experimental pain during static and dynamic tasks. These studies indicate that local excitation of nociceptive afferents has an inhibitory effect on the painful muscle which is counteracted by the reorganization of the motor strategy at the level of the muscle groups involved in the task, which may be viewed as a compensatory mechanism to allow similar motor output in painful and non-painful conditions. This study demonstrates that nociception induces an immediate reduction in the activity of the deep cervical muscles, which is consistent with these previous studies and previous clinical hypotheses.
Compensation by an increased activity of the sternocleidomastoid was seen on the contralateral side of pain induction. Falla et al. (2007) demonstrated that following injection of the sternocleidomastoid muscle, the EMG signal of the splenius capitis muscle was significantly lowered on the side of injection, indicating a reduced activity of this muscle ipsilateral to the side of pain. This reduction was compensated by an increase of synergistic or antagonistic muscle activity. This reorganization may reflect a change in the neural strategy to permit motor and force output to be maintained in the presence of pain, by redistributing loads between synergists and antagonist muscles specific to the performed task. Increased activity was only observed at the C6–C7 level. This may not be surprising as at that level the sternocleidomastoid has a flexion moment arm, in contrast to an extension moment arm at the upper cervical region.
The observed alterations in muscle activity during craniocervical flexion by this experimental model reproduce the changes in control that have been identified in clinical populations. Reduced activity of the deep cervical flexors that coincides increased activity of the superficial flexors have been demonstrated in different neck pain population groups. This reorganization may be interpreted as an efficient and effective strategy in the short term to avoid disruption of the task. It is hypothesized that, in the long term, this reorganization may cause some muscles to experience overload and, as a consequence injury, while causing other muscles to have reduced activity with consequent atrophy. This may contribute to the development of chronic symptoms and partially explain the morphological and histological changes documented in the cervical muscles in persons with traumatic neck pain.
From a clinical perspective, this study supports some key theoretical points for the rehabilitation of muscle impairment in patients with neck pain. This study further highlights the need for specificity in therapeutic exercise selection. Clinical trials have shown that a low-intensity exercise regime designed to train the deep cervical flexors, in contrast to higher-intensity strength and endurance training, is effective at increasing the activation and timing of the deep cervical flexor muscles. In addition, this experimental pain study demonstrates an immediate onset of muscle changes due to pain. This knowledge may support recommendations for the early treatment of patients with neck pain to counteract these changes in motor function with the ultimate aim of minimizing recurrences of neck pain.
This is the first study that indicates an immediate reduction in activity of the deep cervical flexors in response to pain. Consistent with observations in clinical neck pain populations, this reduction in activity coincided with elevated activity of the superficial neck flexors suggesting a reorganization of neuromuscular control in the presence of pain to permit the continuation of the craniocervical flexion motor task. The findings of this study support clinical recommendations regarding the need for early and specific consideration of neuromuscular control when managing patients with neck pain.