Abstract
The purpose of the study was to compare the co-activation of cervical agonist and antagonist muscles between people with chronic tension-type headache (CTTH) and healthy controls during brief isometric cervical flexion and extension contractions. Nine women with CTTH and 10 matched controls participated. Surface electromyographic (EMG) signals were detected from the sternocleidomastoid and splenius capitis muscles bilaterally during cervical flexion and extension contractions of linearly increasing force from 0% to 60% of the maximum voluntary contraction (MVC) in 3 s. Sternocleidomastoid and splenius capitis EMG average rectified values (ARV) were estimated at 10% MVC force increments. During cervical extension contraction, sternocleidomastoid (i.e. antagonist muscle) ARV was greater for patients than for controls in the force range 20-60% MVC (P = 0.029). During cervical flexion, the left splenius capitis (i.e. antagonist muscle) ARV was greater for CTTH patients regardless of the force level (P = 0.02). Maximum cervical flexion and extension force was lower for the CTTH patients compared with controls (P = 0.001). In conclusion, women with CTTH demonstrated greater co-activation of antagonist musculature during cervical extension and flexion contractions compared with healthy women. Increased co-activation of antagonist musculature may reflect reorganization of the motor control strategy in CTTH patients, potentially leading to muscle overload and increased nociception.
Keywords
Introduction
Since primary headaches constitute a major health problem, there has been increasing interest in their pathogenic mechanisms. Tension-type headache is the most common type of headache (1), with a 1-year prevalence rate of 38.3% for the episodic form, and 2.2% for the chronic form (2). In addition, the prevalence of tension-type headache has increased in recent years (3).
The pathogenesis of tension-type headache is still not completely understood. Tension-type headache is a prototypical disorder in which neck-shoulder muscles may play an important aetiological role (4). Referred pain elicited by stimulation of neck flexor and extensor muscles contributes to the pain pattern in chronic tension-type headache (CTTH) (5, 6). Muscle referred pain may be enhanced by sensitization of muscle nociceptors, particularly group III and IV muscle afferents (7), provoked by the release of algogenic substances (bradykinin, serotonin, or substance P) (8). In addition, sensitization of central pathways may facilitate referred pain (9).
Muscle nociceptive afferent activity may alter motor neuron excitability (10). For example, excitation of nociceptive afferents by intramuscular injection of hypertonic saline induces inhibition of muscle activity, characterized by a decrease in motor unit discharge rate (11) and a reduction in the interference electromyographic (EMG) amplitude (12, 13). In addition to a change in activity of the painful muscle, experimentally induced neck muscle pain changes the coordination between cervical agonist and antagonist muscles (14).
Previous studies have assessed alterations in muscle activity in patients with tension-type headache. For example, induced mental stress evokes greater activity in neck and head muscles in CTTH compared with healthy controls (15, 16). Moreover, these patients display a longer recovery time following fatigue of the trapezius muscle compared with controls and people with migraine (17). These findings suggest that motor control strategies are affected in CTTH patients. However, there are also studies that did not show changes in muscle activity in this patient group (18). Such conflicting results may be due to the use of non-standardized tasks for testing muscle function and indicate the necessity for further assessments. Therefore, the aim of this study was to investigate co-activation of cervical agonist and antagonist muscles during cervical isometric contractions in CTTH patients and in healthy controls.
Methods
Subjects
Patients and controls were recruited from advertisement in local newspapers. All patients were interviewed to ensure they met the criteria of the International Headache Society (IHS) for CTTH (19). Of the 15 women with tension-type headache who responded to the advertisement, nine women diagnosed with CTTH [mean ±
Patients received prophylactic, i.e. tricyclic antidepressants, or non-specific anti-inflammatory drugs, but none had received antidepressants at the time the study was completed. Patients were asked to avoid analgesics and muscle relaxants 24 h prior to the examination. All patients were examined when their headache intensity was < 4 on a 10-cm visual analogue scale. Ethical approval for the study was granted by the Local Ethics Committee (VN 2005-0041). Informed consent was obtained from all subjects, and all procedures were conducted according to the Declaration of Helsinki.
Headache characteristics
An 11-point numerical pain rating scale (22, 23) (NPRS; range 0 = no pain to 10 = maximum pain) was used to assess headache intensity. The headache diary was used to calculate the following variables: (i) headache intensity, calculated from the mean of the NPRS of the days with headache; (ii) headache frequency, calculated by dividing the number of days with headache by the number of analysed weeks (days per week); and (iii) headache duration, calculated by dividing the sum of the total hours of headache by the number of days with headache (hours per day).
Electromyography
Bipolar surface EMG was recorded with pairs of electrodes positioned 20 mm apart (Neuroline 72001-k; Medicotest, Olstykke, Denmark) over both the sternocleidomastoid and splenius capitis muscles bilaterally following gentle skin abrasion using abrasive paste. For the sternocleidomastoid muscle, electrodes were placed over the distal portion of the muscle belly (24, 25). For the splenius capitis muscle, electrodes were located over the muscle belly at C2–C3 level between the uppermost parts of sternocleidomastoid and upper trapezius muscle (14). A ground electrode was placed around the subjects' wrist. Myoelectric signals were amplified by 5000 (EMG16, 16-channel amplifier, LISiN-OT; Bioelettronica, Torino, Italy), filtered (–3 dB bandwidth, 10–450 Hz), sampled at 2048 Hz and converted to 12-bit digital samples.
Procedure
Subjects were comfortably seated in a height-adjustable chair of a cervical force measuring device (Aalborg University, Denmark), with their back supported, their knees and hips at 90° of flexion, and their head positioned in a padded head support. The adjustable head support was fastened across the forehead, which stabilized the head and provided resistance during cervical isometric contractions. The electrical signals from the load cells incorporated into the device were amplified (strain gauge amplifier, Aalborg University, Denmark) and their output was displayed on an oscilloscope as visual feedback to the subject.
Following a period of familiarization with the cervical force measuring device and a period to practise the desired contractions, subjects performed three maximum voluntary contractions (MVC) of 3–4 s duration separated by a 1-min rest, for both cervical flexion and extension. Subjects were encouraged to maintain a neutral position of the cervical spine and to perform the flexion and extension contractions maintaining a neutral cranio-cervical and cervical posture. An interval of 5 min was provided between each set of three contractions. Verbal encouragement was provided to encourage the subject to reach a higher force in each trial. The highest value of force recorded over the three maximum contractions for each direction was selected as the reference MVC, and used to calculate the submaximal force targets. The order of the MVC contractions was randomized between movement directions.
After a 10-min rest following the maximal contractions, participants performed, for both cervical flexion and extension, a linearly increasing force contraction from 0% to 60% MVC in 3 s (ramped contraction). A rest of 1 min was provided between contractions that were randomized for force direction.
Signal analysis
The force signal was low-pass filtered (anti-causal Butterworth filter of order 4, cut-off frequency 10 Hz) and normalized with respect to MVC. The average rectified value (ARV) was estimated from the EMG signals over 250-ms windows in which the average force was 10–60% MVC (10% MVC increments). Thus, in both groups the analysed force levels corresponded to the same percentage of maximum force in either cervical flexion or extension.
Statistical analysis
A normal distribution of quantitative data was assessed by means of the Kolmogorov–Smirnov test. EMG data showed normal distribution, whereas headache clinical parameters (i.e. headache intensity, frequency and duration), did not. Subject characteristics (i.e. age, weight, height and BMI) between groups were compared with the Mann–Whitney U-test. Pearson correlation coefficient (r) was computed to analyse linear correlations between clinical variables associated with headache (headache intensity, frequency and duration) within the CTTH group.
A two-way
Results
Headache characteristics
Headache history ranged from 1.5 to 20 years (8.6 ± 6.5 years). The mean headache period per day was 6.3 h (range 3–10 h), the mean intensity (NPRS) per episode was 4.5 (range 3.5–5.5) and the number of days per week with headache was 4.7 (range 4–6 days/week). Mean headache intensity during the experiment was 1.8 (range 0.5–3). No correlation was found between headache history and the other headache clinical parameters. A positive correlation (r = 0.8; P < 0.01) was identified between headache intensity and duration.
Force levels during MVC
Cervical flexion maximum force was lower than maximum cervical extension force for both groups (F = 12.13; P = 0.001; percent difference between flexion and extension 25 ± 16% for CTTH, 35 ± 28% for controls). Women with CTTH demonstrated significantly less force for both cervical flexion (32 ± 10% less than controls) and extension (24 ± 15%) maximum contractions (F = 7.7; P = 0.008).
EMG amplitude
During cervical extension, splenius capitis (agonist) ARV increased bilaterally with increasing force (F = 3.6, P = 0.004); however, there were no differences between patients and controls. During cervical extension, sternocleidomastoid (antagonist) ARV was greater for CTTH patients in the force range 20–60% MVC (F = 2.6, P = 0.029; Fig. 1; Table 1).
Average rectified values of splenius capitis muscles and sternocleidomastoid for cervical extension in patients with chronic tension-type headache (CTTH) and healthy subjects
Values are expressed as percentage of the maximum voluntary contraction in cervical extension with a linear increasing from 10 to 60%.
Mean and standard error of electromyographic average rectified value (ARV) of the sternocleidomastoid and splenius capitis muscles across a linearly increasing cervical extension force contraction from 0 to 60% of the maximum voluntary contraction (MVC). ∗Significant differences between patients and controls (20% P < 0.01; 30–60% P < 0.001).
Across all conditions, both sternocleidomastoid (acting as agonist) and splenius capitis (acting as antagonist) ARV increased with increasing cervical flexion force (F = 120.6, P < 0.001 and F = 29.3, P < 0.001, respectively; Fig. 2). During cervical flexion, left splenius capitis (antagonist) ARV was greater for CTTH patients regardless of the force level (P = 0.02; Fig. 2; Table 2). No group differences for right splenius capitis (antagonist) ARV were identified during cervical flexion (P > 0.05).
Average rectified values of sternocleidomastoid and splenius capitis muscles for cervical flexion in patients with chronic tension-type headache (CTTH) and healthy subjects
Values are expressed as percentage of the maximum voluntary contraction in cervical flexion with a linear increasing from 10 to 60%.
Mean and standard error of electromyographic average rectified value (ARV) of the sternocleidomastoid (acting as agonist) and splenius capitis (acting as antagonist) muscles across a linearly increasing cervical flexion force contraction from 0 to 60% of the maximum voluntary contraction (MVC). ∗Significant differences between patients and controls (P = 0.02).
Discussion
The present study found that women with CTTH demonstrated greater co-activation of an antagonist muscle during cervical extension (i.e. sternocleidomastoid) and flexion (i.e. splenius capitis) contractions compared with healthy women.
Headache clinical features
The clinical characteristics of the included sample of patients were comparable to those reported in previous studies investigating muscle activation in CTTH (15–18). Since the sample of patients with CTTH included in this study was taken from the general headache population, the results may be considered representative of the population of patients with CTTH of moderate intensity. Nevertheless, a small sample size has been used in this study; therefore, generalization of the results should be done with caution. Furthermore, patients with more severe symptoms or suffering from episodic tension-type headache may have different muscular activation. Finally, the duration of headache history of our sample of patients was broad, which may have influenced EMG data and the motor control changes observed.
Muscle co-activation
CTTH women showed reduced force during both cervical flexion and extension contractions compared with healthy women, which is consistent with previous studies (15–17). When the sternocleidomastoid or the splenius capitis muscle acted as an antagonist, the activation was larger in CTTH patients than in healthy subjects. Greater antagonist muscle co-activation occurred bilaterally during cervical extension and unilaterally for cervical flexion, possibly due to the lower absolute force levels during cervical flexion. Another possible reason for unilateral activation during cervical flexion may be a small rotation component during the flexion test, although this is unlikely since the head support was rigid.
Increased antagonist muscle co-activation reflects reorganization of the motor control strategy, which may be a consequence of the nociceptive barrage, and hence of the central sensitization observed in CTTH (26). Previous studies have found that CTTH sufferers exhibit avoidance behaviour and pain-related fear, which is usually seen as a maladaptive process increasing pain-related disability (27–29). Pain-related fear can contribute to changes in muscle use (30) and may explain the observation of increased antagonist activity in the CTTH group.
The greater co-activation of antagonist musculature may also reflect a protective strategy. This hypothesis is in accordance with the pain-adaptation model, which suggests that pain induces reorganisation of the motor strategy characterized by a decrease in agonist muscle activity and an increase in antagonist activity with the aim of limiting the velocity, force and range of movement (31, 32). Both pain and pain-related fear act on motor centres through complex mechanisms (33) and may explain the greater co-activation of cervical flexor and extensor muscles in CTTH patients.
Increased co-activation of antagonist muscles could perpetuate symptoms and contribute towards the chronicity of headache. Overload of both sternocleidomastoid and splenius capitis muscles, caused by an altered motor control strategy, may facilitate the release of algogenic substances, subsequently sensitizing peripheral muscle nociceptors (8) and eventually driving central sensitization. In agreement with this hypothesis, referred pain elicited from cervical flexor and extensor muscles has been shown to contribute to head pain perception in CTTH patients (6). Central sensitization may be the result of prolonged nociceptive barrage from those muscles innervated by the trigeminal nucleus caudalis (34). Therefore, both peripheral and central sensitization may be associated with motor control changes in CTTH.
Clinical significance
Greater co-activation of the superficial neck flexor and extensor muscles may result in excessive compressive loads on the cervical facet joints, thus affecting the biomechanics of the head and the neck (35). Although therapeutic exercise protocols emphasizing motor control retraining have been advocated in randomized controlled trials for effective management of cervicogenic headache (36), there are limited studies assessing the effectiveness of therapeutic exercise interventions in patients with CTTH (37). Two studies have recently found that the inclusion of specific exercises within a physical therapy programme is effective in the management of patients with tension-type headache (38, 39). In particular, the inclusion of an exercise programme focused on the cranio-cervical flexor muscles induced a reduction of symptoms over a prolonged time frame in subjects presenting with tension-type headache (39). Based on the findings of this study, motor control retraining may be an important aspect of the rehabilitation of people with CTTH.
Limitations
The small sample size used in this study may have resulted in type II errors. However, significant differences were observed between patients and controls, which suggests that a greater sample size would not have altered the direction of the findings, but rather have strengthened the current findings.
Conclusions
CTTH women exerted lower maximal forces in cervical flexion and extension contractions than healthy controls. Moreover, they showed greater co-activation of antagonist muscles during cervical extension (i.e. sternocleidomastoid) and flexion (i.e. splenius capitis) contractions compared with healthy women. Determination of the clinical significance of these observations in CTTH and the most effective intervention to address these impairments requires the development and testing of specific exercise programmes.
Footnotes
Acknowledgements
This study was supported by a grant received from Sundheds CVU Nordjylland, Denmark. C. Fernández-de-las-Peñas was supported by the Janet G. Travell, MD Memorial Myofascial Pain Training Fund received from the International Myopain Society. D. Falla is supported by the National Health and Medical Research Council of Australia (ID 351678).