Abstract
Introduction
Tension-type headache (TTH) is highly prevalent in the general population, and it is characterized by increased muscle tenderness with increasing headache frequency and intensity.
Aim
The aim of this case-control study was to compare muscle strength in neck and shoulder muscles in TTH patients and healthy controls by examining maximal voluntary isometric contraction (MVC) during shoulder abduction, neck flexion and extension as well as the extension/flexion strength ratio of the neck.
Methods
Sixty TTH patients and 30 sex- and age-matched healthy controls were included. Patients were included if they had TTH ≥8 days per month. The MVC neck extensor and flexor muscles were tested with the participant seated upright. MVC shoulder abduction was tested with the individual lying supine.
Results
Compared to controls TTH patients had significantly weaker muscle strength in neck extension (p = 0.02), resulting in a significantly lower extension/flexion moment ratio (p = 0.03). TTH patients also showed a tendency toward significantly lower muscle strength in shoulder abduction (p = 0.05). Among the 60 TTH patients, 25 had frequent episodic TTH (FETTH), and 35 had chronic TTH (CTTH).
Conclusion
Patients with TTH exhibited decreased muscle strength in the neck extensor muscles, inducing a reduced cervical extension/flexion ratio compared to healthy people.
Keywords
Introduction
Tension-type headache (TTH) is highly prevalent in the general population and has a high socioeconomic impact (1–3). In accordance with the diagnostic criteria from the International Classification of Headache Disorders, second and third editions, of the International Headache Society (ICHD-II, III) (4,5), TTH can be classified by the number of headache days (4,5). In the adult Danish population, frequent episodic TTH (FETTH) and chronic TTH (CTTH) have a prevalence of 37.2% and 4.8%, respectively (2). The origin of TTH is multifactorial (6–8), but the muscular factor is considered to be one of the most important factors. Several studies have shown increased tenderness in pericranial myofascial tissues (9,10). TTH has the characteristic of increased tenderness with increasing headache frequency and intensity, which is not found in migraine patients (6). In a large-scale population-based study from Norway, a positive association between headache and musculoskeletal symptoms was identified with a four times higher prevalence of chronic headache in individuals with musculoskeletal symptoms compared to participants without such symptoms (11). Further, the study found a high association between neck pain and headache. This was confirmed in a study from Denmark that found that neck pain in individuals with TTH was more common than in the general population (12). In the understanding of pathophysiological mechanisms in TTH, the potential role of the peripheral muscles is considered as one of the most important but yet undisclosed issues.
Fernández-de-las-Peñas et al. have in a number of studies demonstrated that CTTH is associated with trigger points in the suboccipital, upper trapezius, sternocleidomastoid muscles (13–15). These muscles are all involved in the movement of the neck. Furthermore, they found that the cross-sectional area of the rectus capitis posterior minor was smaller in CTTH patients with active trigger points, in a small study with 11 CTTH females (16). Trigger points are, by Simons et al., defined as a hyper-irritable spot within a taut band of skeletal muscle (17). Jull et al. (18) examined the function of the neck in frequent headache patients with ≥1 headache day per month in TTH, migraine or cervicogenic headache, as well as in healthy controls. They found no significant reduction in maximal voluntary contraction (MVC) in the TTH group (18). MVC is the maximum force produced in a specific isometric exercise. In another study by Fernández-de-las-Peñas et al., the neck strength tests of nine CTTH patients and 10 healthy controls demonstrated a significantly reduced strength in both flexion and extension of the neck muscles in the CTTH group and in addition showed a significantly increased coactivation of the antagonistic neck muscles (19). The difference in neck strength deficits found in FETTH and CTTH elucidates the importance of clarification of the neck strength in TTH patients. Identifying a compromised ability to generate force and provide stability in the neck can contribute to elucidate functional causes or consequences of TTH. Therefore, the relation between the maximal strength in neck flexion and extension may also be important for the role of neck flexor and extensor muscles in TTH.
The most common tender muscles in TTH are the lateral pterygoid, the sternocleidomastoid and the descending part of the trapezius (9,20). Functionally, the trapezius muscle is of major importance both in neck extension and in shoulder abduction, and therefore of major interest to investigate in TTH (21,22). At present it is unknown if TTH presents a reduced ability to generate force over the shoulder joint.
Aim
The aim of this case-control study was to compare the muscle strength in neck and shoulder muscles of TTH patients and healthy controls. It was hypothesized that the TTH group would have a reduced MVC in shoulder abduction, neck extension and flexion as well as a reduced neck extension/flexion ratio compared to healthy controls.
Materials and methods
Participants
TTH patients were recruited from the Danish Headache Center, Department of Neurology, Glostrup Hospital and the headache clinic, Department of Neurology Bispebjerg Hospital, Copenhagen, tertiary and secondary headache centers, respectively. Additional TTH patients and the healthy controls were included from a Danish Web page for trials (www.forsoegsperson.dk) or from our database in the Danish Headache Center. Inclusion criteria were age between 18 and 65 years and for patients a diagnosis of TTH ≥8 headache days per month (FETTH or CTTH), and ≤3 migraine days per month according to ICHD-II criteria (4). All interested participants were asked to fill out a headache diary for four weeks before their first consultation at the hospital. They were included in the study only if the participants complied with this demand and if the diary met the ICHD-II criteria for TTH. If the diary was inconclusive regarding days of migraine and TTH, the diary data were supplemented with a consultation with a headache specialist and a detailed diagnostic telephone interview with the patient.
Exclusion criteria for the healthy controls were physical or mental illness, and history of significant headache (i.e. more than 12 headache days per year). Exclusion criteria for the patients included medication-overuse headache (ICHD-II), previous whiplash or head trauma, or other major physical or neurological diseases. The patients were tested for cervicogenic headache according to Jull et al. (18), and were excluded if the test was positive. The patients and controls were excluded if they were diagnosed with depression, or other mental illness, or if they were unable to understand and speak Danish. The healthy controls were sex and age matched to the TTH patients. A flowchart of the participants in the study is shown in Figure 1.
Recruitment process.
The study forms the baseline for a randomized, controlled trial (RCT) with specific strength training as intervention for the included TTH patients. For ethical and practical reasons we used the following calculation for the participants. The number of participants in the present study was estimated based on power calculations for a subsequent intervention trial. It was estimated that a clinically relevant change in headache frequency is δ = 30%, and that the standard deviation for deciding the frequency is s = 40%. Accepting a risk of type 1 error of 5% and a risk of type 2 error of 20% (Figure 15.2 in Altman (23)), it was estimated that the necessary number of participants in each group was 25. Allowing for a dropout, the study was dimensioned to 30 healthy controls and 30 people in each patient arm, namely the intervention group and the patient control group. In the present case-control study, we therefore aimed to include 60 TTH patients and 30 healthy age- and sex-matched controls. The healthy controls did not participate in the RCT, and they exited the trial after the baseline case-control testing.
The participants received written and verbal information about the study, and all participants gave written informed consent. The patients and healthy controls were included over a period of two years from 2010 to 2012 (Figure 1). The patients were included by the physiotherapist (BKM) and tested by an independent examiner (HA). The physiotherapist was blinded to the test result, and we aimed to keep the examiner blinded to the headache status. Ethics approval for the study was granted by the ethics committee of the Capital Region of Denmark: H-3-2009-080.
Measurements
The strength tests were conducted as a baseline screening with several tests in a standardized test battery with the same tester for all measurements. If patients had migraine on the test day, the testing was rescheduled, whereas ongoing TTH pain did not prevent testing. All MVC tests were performed using a computerized system including a force transducer from Vishay Nobel (type KIS-2, max. 2 kN) and a signal conditioning unit from National Instruments, type PWR02 (including a strain gauge amplifier, type SCC-SG24), and a data acquisition card, Daqcard-6036E. The signals were sampled with a frequency of 100 Hz and low-pass filtered with a cut-off frequency of 10 Hz.
Cervical muscle strength
Maximal isometric force in the neck extensor, and flexor muscles were measured with the participant seated in an upright position on a chair with the chest strapped to a vertical plate and arms hanging relaxed in front of a custom-designed steel frame with an attachment arm and a strain gauge force transducer as seen in flexion (Figure 2). For neck extension as seen in Figure 3, the participant sat upright with the back of the head in front of the transducer. The transducer attachment arm was individually adjusted in height, so the back of the head touched the dynamometer at the protuberantia occipitalis. The distance between C7 and protuberantia was measured and used as the moment arm for the extension moment.
Position for measuring of flexion. Position for measuring of extension.
To test neck flexion, the participant sat with the forehead in front of the dynamometer. The transducer attachment arm was adjusted in height so the head touched the dynamometer at the level of the eyebrows. The adjustment of the dynamometer was registered and added or subtracted from the extension moment arm and used as the moment arm for the flexion moment.
The participants were instructed to slowly build up the force to maximal strength within two seconds, and then exert maximal pressure for about three seconds and thereafter slowly relax. Participants were verbally encouraged to perform maximally. A test trial was conducted, and a further three trials were conducted. If there was a >5% difference in peak force among these three attempts, up to five additional trials were conducted. A 30-second rest was allowed between each attempt. The moment of neck extension and flexion force was calculated as peak force*moment arm and the extension/flexion ratio as the ratio between the calculated extension and flexion moment.
Using the same equipment, testing of isometric shoulder muscle strength was subsequently performed (Figure 4). The placement of the dynamometer in the custom-designed steel frame was adjusted, enabling the test person to be tested lying supine. The test person lay with the arm in a 90-degree abducted angle and 15 degrees from the frontal plane with the elbow slightly bent and the arm not touching the floor. The wrist (processus styloideus radii) was placed in the middle of the force plate and the distance from acromion to processus styloideus radii was measured and taken as the moment arm for the abduction moment. The test person was instructed to press as fast and forcefully as possible in the direction of abduction. A test trial was conducted and three attempts were made. If there was a >5% difference, up to five extra attempts were conducted. A 30-second rest was allowed between each attempt. The trial with the highest MVC peak force measure was registered as the individual's abduction MVC force and used for calculation of the moment. The moment of shoulder force was calculated as peak force*moment arm.
Position for measuring of abduction. Mean (SE) neck flexion, shoulder abduction, neck extension, neck extension/flexion (Nm) for TTH compared to controls. * p < 0.05.
Headache
Frequency, intensity and duration of headache were registered in a headache diary. Duration of the headache was registered in hours on each day with headache. The intensity was registered on a 0–10 numeric rating scale (NRS) where 0 is no pain, and 10 is worst possible pain. Additional characteristics of the headache were registered and used for diagnosing the headache as days of TTH or migraine. On the test day the headache intensity was registered as 0–10 on a visual analog scale (VAS).
Statistics
Stata (Stata release 12, StataCorp LP, USA) was used to calculate statistics. In anthropometric measures the normal distribution could not be confirmed by Shapiro-Wilk W test, and a non-parametric Mann-Whitney test was used to examine any significant difference between groups. For all other comparisons, when Shapiro-Wilk W test concluded that test data were not normally distributed, data were log transformed, and a t-test was used to test for significant difference between healthy controls and TTH as well as for testing differences between TTH with and without migraine in a subgroup analysis. For subgroup analysis of FETTH and CTTH, we used analysis of variance (ANOVA).
P < 0.05 was used as the level of significance. In the text data are presented as mean ± standard deviations unless otherwise described. Diagrams are presented with standard errors of mean (SE).
Results
Age and anthropometric measures of included participants.
TTH: tension-type headache; BMI: body mass index: weight/height2. Mean (SD) N = 90a study population: whole population (females).
Headache characteristics of included TTH patients.
TTH: tension-type headache; NRS: numeric rating scale; VAS: visual analogue scale. Mean values and SD are presented.
There was a significant difference in the neck extension moment between TTH patients (17.07 ± 9.16 Nm) and controls (21.49 ± 10.31 Nm) (p = 0.02), Figure 5. In contrast, there was no significant difference in neck flexion moment between TTH patients (11.40 ± 5.66 Nm) and controls (12.79 ± 5.83 Nm) (p = 0.1). The lower extension moment resulted in a significantly lower extension/flexion moment ratio for TTH (1:1.54) compared to controls (1:1.72) (p = 0.03). Regarding shoulder abduction moment, a borderline significant difference was found between the two groups (38.7 ± 15.9 vs. 44.3 ± 19.3 Nm) (p = 0.05), Figure 5.
There were no significant differences between the TTH patients with and without migraine in any of the described tests. For TTH without migraine and TTH with migraine, respectively, extension moments were (17.38 ± 9.14) vs. (16.05 ± 9.51) Nm (p = 0.65), and flexion moments were (11.58 ± 5.86) vs (10.81 ± 5.08) Nm (p = 0.92). Extension/flexion ratios were (1:1.50) (p = 0.47), and shoulder moments were (39.27 ± 17.20) vs (36.64 ± 10.78) Nm (p = 0.49). A subgroup analysis for possible differences between FETTH and CTTH showed no significant differences in extension moment (p = 0.13), flexion moment (p = 0.47), abduction moment (p = 0.36) or extension/flexion ratio (p = 0.28).
Discussion
In this study it was hypothesized that the TTH group would have a generally lower MVC in neck extension and flexion muscles as well as a lower extension/flexion ratio, and shoulder MVC compared to healthy controls. The hypotheses were partly confirmed as TTH patients had a reduced strength in neck extension muscles, with the control group being 26% stronger than the TTH group. In contrast, no difference was found for neck flexion muscles between TTH and healthy controls. Further, it was confirmed that there was a lower extension/flexion ratio in the TTH group with a 12% larger ratio in the healthy controls. A borderline significant difference in the ability to generate muscle force over the shoulder joint was found, with the controls showing a 15% higher shoulder abduction moment. During testing the participants rested 30 seconds between testing in order to avoid fatigue. This was estimated as sufficient time to recover from the previous test. The TTH patients with coexisting migraine were similar to the patients with pure TTH in all force variables, and can therefore not be considered as a specific subgroup.
Muscular aspects in TTH
In a study with female office workers with chronic trapezius myalgia, it was found that the maximal force capacity of the shoulder was 18% higher in the healthy controls (22). Similarly, the TTH patients in the present study display the same characteristics as the trapezius myalgia group, in terms of impaired ability to generate force. The trapezius muscle has an important function in both neck extension and shoulder abduction. A tender trapezius could be a plausible causal explanation for both the extension and abduction muscles being affected in the TTH group. Fernández-de-las-Peñas et al. have demonstrated an association of CTTH with trigger points in the suboccipital, upper trapezius and sternocleidomastoid muscles (13–15). These muscles are all involved in the movement of the neck. Further, the cross-sectional area of the rectus capitis posterior minor was found to be smaller in CTTH patients with active trigger points (16). The presence of active trigger points could potentially explain some of the reduced force in the neck extensor muscles. If further studies can confirm the atrophy found in capitis posterior minor with active trigger points, this could also contribute to a reduced strength in extension. Muscle pain may cause reduced motor performance, with decreased neural drive during maximal voluntary muscle contraction (24). In the present study, we found a reduced extension/flexion ratio in the TTH group, primarily due to relatively weaker extension muscles compared to healthy controls. Jordan et al. found the ratio to be 1:1.7 in a normal population, which is completely in line with the ratio of 1:1.72 for the healthy controls in the present study (25,26). The lower ratio of 1:1.54 found in the TTH group indicates that a higher relative loading of the neck extensor muscles could be present in everyday activities. This possibly contributes to additional tension in the extensor muscles as well as disturbed stabilization in the neck and coordination of head movements. Fernández-de-las-Peñas et al. (14,27) found in their case-control studies a significantly different forward head posture in TTH patients compared to healthy controls. The forward head posture may be related to a reduced extension/flexion ratio in muscle strength as found in the present study. The lower ratio, and possibly changed loading in everyday life, could lead to an earlier recruitment of fast twitch fibers, faster fatigability and more tension in these muscles (28). This could cause a maintained muscle activity with gradually more painful muscles, over time potentially leading to CTTH in accordance with the model described by Bendtsen in 2000 (9).
In this model an induced and maintained continuous painful input is suggested to lead to central sensitization, where stimuli that are normally not painful are misinterpreted and perceived as painful (9). It is thus possible that with further chronification of headache, central sensitization could influence the ability to generate additional force and more muscle groups would be affected over time.
Anatomical aspects of TTH
Anatomically, there is a convergence between the afferent nerves of the upper three cervical nerves (C1 to C3) and trigeminal afferents, and therefore pain from the upper cervical structures can be perceived as pain in the frontal region of the head (29,30). Among the structures and muscles innervated by the three nerves is the trapezius, which therefore potentially can contribute to TTH. It is therefore interesting that the results in the present study confirm the deteriorated force-generation capacity specifically in the strength measures that involve the trapezius muscle, while the flexion muscle strength seems unaffected, excluding a general muscle weakness.
Clinical significance
A reduced extension/flexion ratio may potentially contribute to TTH onset and over time the development of CTTH. Ettekoven et al. (31) applied an intervention consisting of posture correction and motor control training of the neck over a six-week period and presented a highly significant reduction of TTH frequency with (50% or more) for 82% of participants at the end point (week 6) and 85% at follow-up (month 6). A possible explanation for this reduction could be a normalization of the extension/flexion ratio; however, these data were not provided. Further, a registration of active trigger points in the neck muscles, could also contribute to the understanding of the motor control mechanisms in TTH. Another approach to normalization of the extension/flexion ratio and a reduction of TTH could be specific strength training of the trapezius muscle (32). Normalizing the reduced strength of both extension and abduction found in this study. Though a concern could be that strength training could contribute to a further sensitization, further research is needed to understand the effect of strength training on TTH. There is though evidence of an effect on TTH and neck shoulder pain with strength training in office workers (33).
Strength and limitations
The strength of the study was the precise classification of patients and the blinded systematic design. Lindstroem et al. (34) showed that fear avoidance of pain in neck pain could explain some of the reduced MVC found in neck pain patients. A limitation of our study was that any associations between neck pain characteristics and eventual fear of pain were not registered. We therefore cannot clarify if the pain's influence on the MVC is through an influenced neural drive, fear avoidance, or other properties of the muscles. Further, a registration of headache and neck pain during testing could have contributed to a further understanding of the group's response to the use of neck and shoulder muscles. A registration of exercise habits could more precisely show if the two groups are similar, and except for TTH, are comparable. Furthermore, causality cannot be determined as the present study is cross-sectional so it is uncertain whether the present results are causal or an effect of local pain or TTH. Hopefully, the results of the forthcoming intervention study involving the cases in the present case-control study may further add to our understanding of the role of muscle strength in TTH. The relatively large number of patients in the TTH group who were excluded (Figure 1) was mainly due to the lack of ability to complete the diary, and their response to contact. A limitation to the study is that not all the patients did register their full headache status or reason for lack of compliance. As those not complying with this request were excluded, we have limited knowledge of the excluded group and the external validity of the results in the study.
Conclusion
Lower extension strength, extension/flexion ratio, and borderline lower shoulder abduction strength were identified in patients with TTH compared to healthy controls. The cause-effect relation remains, however, spurious. The results lend support to the hypothesis that specific training of the weak trapezius muscle may contribute to a normalization of the strength in neck and shoulder in the TTH patients. This may potentially lead to reduced TTH, but this remains to be shown in a prospective design.
Clinical Implications
In the present study we found a reduced extension/flexion ratio in the tension-type headache (TTH) group, primarily due to relatively weaker extension muscles compared to healthy controls. Reduced muscle strength could indicate unbalanced muscle activity in TTH patients that can contribute to TTH and over time lead to chronification. Specific training of the weak trapezius muscle may contribute to a normalization of the strength in the neck and shoulder in TTH patients and may potentially lead to a reduced TTH.
Footnotes
Conflict of interest
None declared.
Funding
The work was supported by The Tryg Foundation.