Volume 85, Issue 10 , Pages 1684-1688, October 2004
Decreased neck muscle strength is highly associated with pain in cervical dystonia patients treated with botulinum toxin injections1
Article Outline
Abstract
Häkkinen A, Ylinen J, Rinta-Keturi M, Talvitie U, Kautiainen H, Rissanen A. Decreased neck muscle strength is highly associated with pain in cervical dystonia patients treated with botulinum toxin injections. Arch Phys Med Rehabil 2004;85:1684–8.
Objectives
To compare the isometric neck muscle strength of cervical dystonia patients treated with botulinum toxin injections with that of healthy control subjects and to evaluate the association between neck strength, neck pain, and disability in these patients.
Design
Clinical cross-sectional study.
Setting
Outpatient rehabilitation and neurology clinics in a Finnish hospital.
Participants
Twenty-three patients with cervical dystonia with botulinum toxin—treated neck muscles and 23 healthy control subjects.
Interventions
Not applicable.
Main outcome measures
Isometric neck strength was measured by a special neck strength measurement system. Disability was measured by the Neck Disability Index, and pain and symptoms of cervical dystonia by a visual analog scale.
Results
Isometric neck strength in all directions measured was significantly lower (25%–44%) in the cervical dystonia patients than in the healthy controls. Neck pain levels reported during the strength tests (r range, −.36 to −.70) and neck pain experienced during the preceding week (r range, −.52 to −.63) were inversely associated with isometric strength results. The difference between sides in rotation strength was 35% in the patient group (P<.001), whereas no significant difference between sides was found in the healthy controls. Fifty-one percent of the patients reported moderate or severe disability. Pain, stiffness, and incorrect position of the head were the most prominent symptoms.
Conclusions
Cervical dystonia patients with botulinum toxin—treated neck muscles showed significantly lower maximal neck strength than healthy controls. The patients also had a statistically significant difference between sides in neck rotation strength. Thus, strength measures may be useful to detect disturbance in the function of the neck muscles.
Keywords: Botulinum toxins, Cervical dystonia, Disabled persons, Neck muscles, Pain, Rehabilitation
IDIOPATHIC CERVICAL dystonia is the most common form of adult-onset focal dystonias.1, 2, 3 The mean age of onset is early in the fifth decade and women are affected 1.5 to 1.9 times more often than men.4, 5, 6 Cervical dystonia is characterized by tonic and intermittent spasms of the neck muscles that typically cause an involuntary deviation of the head from center position.3 Spasm intensity varies according to the state of muscular tension and the position adopted (lying, standing, moving), and patients complain of a pulling or drawing in the neck or an involuntary twisting or jerking of the head. Cervical dystonia often causes difficulties in carrying out everyday activities. In 99% of a sample of 220 patients with cervical dystonia, Rondot et al4 reported some degree of disability, ranging from mild, with a subjective feeling of discomfort in social situations without objective effects on social life, to severe, with qualitative and quantitative modification at the occupational level sufficient to impair social life.
Pain associated with head turning and spasms is reported to be present in 75% of cervical dystonia patients at some point during the illness.1 Patients often consider the pain to be a major source of disability.1, 2, 3, 5 Muscle spasm contributes to an overall shortening of the length of the muscle in question, with increased tone or tension and stiffness. Several earlier studies7, 8, 9, 10, 11 showed that neck strength is lower in patients with chronic neck pain than in healthy controls. Although different types of strengthening and stretching exercises have been recommended for cervical dystonia patients,12 we found no studies on using muscle strength measures to obtain more objective information on decreased function caused by cervical dystonia.
The primary goal of this cross-sectional study was to compare isometric neck muscle strength among cervical dystonia patients treated with botulinum toxin injections with that of healthy control subjects. A second objective was to evaluate the association between the neck pain and disability with neck strength in the same patients.
Methods
Participants
Jyväskylä Central Hospital is the only center in the district of Central Finland (population, 265,000) where cervical dystonia is treated with botulinum toxin. All 28 patients with cervical dystonia (≈1/10,000 inhabitants) who were receiving botulinum toxin injections in their neck muscles in our outpatient neurology clinic were invited by mail to volunteer for the study. Questionnaires were returned by 89% of the patients. Four of responders declined to participate and 1 was excluded from the study, because the symptoms were not only in the neck. Finally, 23 patients were included in the study.
Muscle spasm—induced rotation to the right was in 20 patients, and to the left in 3 patients. The mean amount of time since the diagnosis of cervical dystonia ± standard deviation (SD) was 12.7±9.9 years, and the duration of symptoms before diagnosis was 5.3±7.3 years. During the previous 12 months, 17 (71%) of the patients reported no change, 4 (17%) reported minor improvement, and 3 (12%) reported some worsening of symptoms. Three of the patients had undergone right or left myotomy of the sternocleidomastoid muscle, and 1 of them also had a myotomy of the scalenus anterior muscle.
The mean number of series of botulinum toxin type A (BTX) injections was 14±8. In the majority of cases, 2 to 3 muscles were injected per session. The mean BTX dose per session was 3.8±0.9mL (range, 2–6mL) in a concentration of 25U of BTX/mL. The mean duration between the injections was 2.5±0.4 months (range, 2–3mo). According to the questionnaire, the subjective beneficial effect of toxin was highest in 80% of the patients during the first 2 weeks after injection. In addition to the BTX treatment, 67% of the patients had used pain medication and 50% had used muscle relaxants during the preceding month. Sixty percent of the patients were having various forms of physiotherapy (PT) and 71% of them were doing regular gymnastics at home. The PT mainly consisted of massage, stretching, training to position the head correctly, and relaxation. The home programs included muscle stretching and strengthening exercises, exercises to correct the asymmetrical posture of the neck and upper body, and relaxation.
The control group consisted of 23 healthy volunteers selected locally from the population of the town. They were matched with the patients according to sex, age, weight, and height to eliminate major confounding factors. There were no statistically significant differences in physical characteristics between the groups (table 1). The local ethics committee approved the study and all the participants gave written informed consent after having the study protocol explained to them.
Table 1. Demographic Data of Patients With Cervical Dystonia and Healthy Controls
| Patients (n=23) | Controls (n=23) | |
|---|---|---|
| Female/male | 17/6 | 17/6 |
| Age (y) | 54±14 | 54±13 |
| Weight (kg) | 69±14 | 73±13 |
| Height (cm) | 166±7 | 167±8 |
| Body mass index (kg/cm2) | 25±4 | 27±4 |
Measurements
Neck function was assessed by measuring maximal isometric strength and mobility of the cervical spine. The reliability of the device specially designed for the clinical measurements of neck strength was evaluated in an earlier study (intraclass correlation coefficient range, .89–.98).13 The isometric rotation strength was measured against torsion forces applied to the axis of the Neck Strength Measurement Systema (NSMS). In this test, subjects attempted to rotate their heads against the head supports, first to the right and then to the left. Next, for the flexion and extension measurements, subjects pushed against the padded strain gauge of the NSMS (fig 1). Subjects made at least 3 maximal efforts in all directions after 2 to 3 warm-up efforts. If the third result was more than 5% better than the previous 2 results, extra trials were performed until the improvement in strength remained under 5%. The best result was used in the final analysis. Pain felt during the strength measurements in different directions was assessed by a 100-mm visual analog scale14 (VAS). Maximal isometric grip strength was measured by a Jamar standard dynamometer.15,b
Fig 1.
Positioning of the subjects during the strength measurements in the isometric neck strength testing machine. The chest and waist were held with broad straps to eliminate contribution of the trunk musculature.
Disability was measured by the Neck Disability Index (NDI), which consists of 10 sets of questions on the activities of daily living, each to be answered according to a 5-point scale.16 Pain, neck and shoulder region numbness, stiffness and tremor, and incorrect head position were assessed by VAS. In that series of questions, a score of 0 denoted no pain or symptom, whereas a score of 100 indicated the highest level of pain and worst possible symptoms. Assessments of patients’ physical function and subjective outcome were scheduled for the same day before the administration of the BTX injection. This day was selected on the assumption that the symptoms of cervical dystonia would be at their most pronounced during that time.
Statistical methods
The results are expressed as means with SDs and medians with interquartile ranges. The normality of the variables was evaluated by the Kolmogorov-Smirnov test, with Lilliefors significance. Statistical comparisons between the study groups were performed by the unpaired t test or by the Well test when appropriate. In the multivariate analysis of the muscle strength results, the Hotelling T2 method for generalized means was used. The most important descriptive values were expressed with a 95% confidence interval (CI). The Pearson correlation coefficient was used to evaluate the relationships between the variables. The α level was set at .05.
Results
Mean pain experienced during the preceding 7 days in the cervical dystonia patients was 52±29mm and NDI score was 15±8. In 48% of the patients (n=11), the disability was mild, in 43% (n=10) moderate, and in 9% (n=2) severe. Of the patients, half reported that their physical symptoms limited their social life. The problems subjectively perceived by the patients as associated with cervical dystonia are in table 2.
Table 2. Subjectively Perceived Intensity of Symptoms on VAS (0–100mm) in 24 Patients With Cervical Dystonia
| No. Patients With Symptoms | Mean ± SD | Range | |
|---|---|---|---|
| Incorrect head position | 23 | 56±26 | 13–94 |
| Head tremor | 21 | 44±33 | 1–92 |
| Pain in neck and shoulder region | 23 | 54±30 | 1–96 |
| Stiffness in neck and shoulder region | 23 | 55±29 | 1–96 |
| Numbness in neck and shoulder region | 15 | 40±33 | 2–100 |
Isometric neck strength was significantly lower in all the directions measured in the patients compared with healthy controls (Hotelling T2, P=.012) (table 3). The relative mean difference between the sides in rotation was 35%±25% in the patients (P<.001), whereas the difference of 12%±8% found in the healthy controls was statistically nonsignificant. Wide individual variation of neck rotation strength was found in the patients (fig 2). The flexion/extension ratio of .73 in cervical spine muscle in the patients was comparable with the ratio of .75 found in healthy controls. The mean grip strength of the patient group (282±128N) did not differ significantly from that of the healthy controls (339±106N).
Table 3. Mean Maximal Isometric Neck Muscle Strength in Patients and Controls
| Neck Muscle Strength | Patients (n=23) | Healthy Controls (n=23) | Difference Between Groups (95% CI)∗ |
|---|---|---|---|
| Flexion (N) | 64.3±50.1 | 87.8±35.5 | −23.5 (−49.1 to −2.1) |
| Extension (N) | 151.8±94.9 | 202.4±70.0 | −50.6 (−99.7 to −1.4) |
| Right rotation (Nm) | 5.8±4.7 | 9.6±4.1 | −4.2 (−6.4 to −1.2) |
| Left rotation (Nm) | 6.4±5.9 | 9.2±4.3 | −3.0 (−6.8 to −0.3) |
∗ Hotelling trace in neck strength, P=.012. |
Fig 2.
Difference between sides in neck rotation strength in patients with cervical dystonia and in healthy controls. NOTE. Circles show the mean and whiskers the 95% CIs.
Ten patients reported pain (mean, 53±30mm) during the strength test of flexion, 3 during extension, and 7 and 5, respectively, during rotation to right and left. The neck strength results were inversely associated with the amount of neck pain reported during each measurement (r range, −.36 to−.70; 95% CI, −.86 to −.06). Further, pain experienced during the preceding week was associated with the results of neck strength (r range, −.52 to −.63; 95% CI, −.82 to −.15). No pain was reported by the healthy controls.
Table 4 shows the proportion of patients who reported alleviation of their cervical dystonia symptoms after different treatment modalities. Use of muscle relaxants, number of BTX injections, PT, or home exercises were not associated with the neck muscle strength results, whereas the use of pain medication showed an inverse association (r range, −.49 to −.56; 95% CI, −.79 to −.11). The NDI was also associated with the neck strength results (r range, −.59 to −.67; 95% CI, −.85 to −.25), with neck pain (r=.60; 95% CI, .26–.81), with incorrect position of the neck (r=.62; 95% CI, .29–.82), with neck stiffness (r=.57; 95% CI, .22–.79), and with neck tremor (r=.52; 95% CI, .15–.76).
Table 4. Percentages of Cervical Dystonia Patients Reporting Subjectively Perceived Benefits From Different Treatments
| Botulinum Toxin (n=24) | Muscle Relaxants (n=12) | Painkillers (n=16) | Home Exercise (n=21) | PT (n=15) | |
|---|---|---|---|---|---|
| Incorrect position of the head | 100 | 83 | 19 | 71 | 60 |
| Head tremor | 81 | 91 | 21 | 58 | 62 |
| Pain in neck-shoulder region | 88 | 75 | 88 | 86 | 87 |
| Stiffness in neck and shoulder region | 92 | 92 | 63 | 91 | 87 |
| Numbness in neck and shoulder region | 87 | 36 | 22 | 73 | 89 |
Of the 4 patients who had been treated surgically, 3 had obtained some relief for incorrect position of the head, 2 for pain and stiffness, and 1 for numbness in the neck and shoulder region; but all 4 still needed BTX treatment. Further, isometric neck strength values were 16% to 27% lower in all the directions tested in these patients compared with patients on BTX treatment only. However, because of wide individual variation, the differences between the groups were not significant.
Discussion
The results indicate that isometric neck strength was significantly lower in all the directions measured in cervical dystonia patients treated with BTX injections compared with healthy controls. Patients also had a statistically significant difference between sides in rotation strength, which showed the imbalance between right and left rotator muscles. The healthy subjects had no statistically significant differences between sides. Tonic muscular contraction may shorten both the length of the muscles and the moment arm and thus affect muscle function. At the doses used in these patients, BTX injections cause partial paralysis of the muscles injected. It may also cause a reduction in neck muscle strength as well as differences between sides.
Although maximal muscle strength was lower in the patient group, their flexion/extension strength ratio was comparable to that of the healthy subjects. Thus cervical dystonia seems to have comparable effects on neck flexion strength and extension muscle strength. In everyday life, the neck extensor muscles have to support the head in an upright position against the forces of gravity and thus there is a great difference in muscle strength between the posterior and anterior muscles. The condition itself, together with pain, affects the movements of the head in the long term, leading to a reduction in the amount and intensity of everyday physical movement, and thus to a reduction in the use and maximal strength of the neck muscles.4 Further, neck muscle myotomies showed a tendency to reduce neck muscle strength, although the results were not statistically significant because of the low number of surgically treated patients.
The reason for using BTX in the clinical management of dystonia is to reduce pain and the focal or abnormal spasticity of muscle. The present patients were assessed at the moment when the cervical dystonia would be at its worst because the longest possible period had elapsed since the last BTX injection. The most reported symptoms were pain, incorrect head position, and numbness in the neck and shoulder region. In earlier studies,1, 2 pain incidence was reported to be 75%, but these studies also included patients with mild cervical dystonia, whereas the present study consisted only of patients with more severe symptoms who were receiving BTX treatment. However, the decrease in neck strength8, 17, 18 and level of pain19, 20 in these patients was similar to that reported earlier in patients with chronic neck pain, with 1 exception: the other chronic neck pain patients did not have an imbalance between right and left rotator muscles.9, 10, 11 On the other hand, even long-term BTX treatment in cervical dystonia patients does not seem to cause higher strength reduction compared with chronic nonspecific neck pain. Nevertheless, pain may in part prevent maximum muscle contraction during strength tests and reflex inhibition may prevent the production of maximal force levels.21 Thus, in patients with cervical dystonia and other chronic neck pain conditions, the test results do not always describe true maximal strength. Results are also affected by patients’ ability to bear strain—a factor that may be considerably influenced by their experience of pain.
Conclusions
To our knowledge, this study is the first to report on the characteristics of neck muscle strength in patients receiving BTX treatment. The present patients had significantly decreased maximal strength and a higher difference between sides in rotation strength as compared with healthy controls. Pain was highly associated with impaired neck strength results. Because individual variation in the strength results was wide in the patient group, neck strength measures are recommended as a way to detect possible weakness and imbalance of the neck muscles.
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References
- . Idiopatic cervical dystonia (clinical characteristics). Mov Disord. 1991;6:119–126
- . Natural history of adult-onset idiopathic torticollis. Arch Neurol. 1990;47:548–552
- . The clinical course of spasmoidic torticollis. Neurology. 1988;28:530–532
- . Spasmodic torticollis—review of 220 patients. Can J Neurol Sci. 1991;18:143–151
- . Cervical dystonia (clinical findings and associated movement disorders). Neurology. 1991;41:1088–1091
- . Current concepts on the clinical features, aetiology and management of idiopathic cervical dystonia. Brain. 1998;121:547–560
- Pattern of premature degenerative changes of the cervical spine in patients with spasmodic torticollis and the impact on the outcome of selective peripheral denervation. J Neurol Neurosurg Psychiatry. 2000;68:465–471
- . A comparison of physical characteristics between patients seeking treatment for neck pain and matched healthy individuals. J Manipulative Phys Ther. 1997;20:468–475
- . Evaluation of cervical range of motion and isometric neck muscle strength (reliability and validity). Clin Rehabil. 2002;16:851–858
- . Decreased strength and mobility in patients after anterior cervical diskectomy. Arch Phys Med Rehabil. 2003;84:1043–1047
- . Cervicobrachial syndrome and neck muscle function (effects of rehabilitation). J Musculoskeletal Pain. 1993;1:283–288
- . In: Spasmoidic torticollis. Handbook of rehabilitative physiotherapy. Paris: Editions Frison-Roche; 1994;p. 5–15
- . Reproducibility of isometric strength measurement of neck muscles. Clin Biomech (Bristol, Avon). 1999;14:217–219
- . Reproducibility along a 10-cm vertical visual analogue scale. Ann Rheum Dis. 1981;40:87–89
- . Reliability and validity of grip and pinch strength measurements. Crit Rev Phys Rehabil Med. 1991;4:201–212
- . The neck disability index (a study of reliability and validity). J Manipulative Physiol Ther. 1991;14:409–415
- . Neck flexor muscle strength, efficiency, and relaxation times in normal subjects and subjects with unilateral neck pain and headache. Arch Phys Med Rehabil. 1996;77:680–687
- . Maximal isometric muscle strength of the cervical spine in healthy volunteers. Clin Rehabil. 2002;16:772–779
- . Active treatment of chronic neck pain (a prospective randomized intervention). Spine. 2000;25:1021–1027
- . Pain, coping, emotional state and physical function in patients with chronic radicular neck pain. A comparison between patients treated with surgery, physiotherapy or neck collar—a blinded, prospective randomized study. Disabil Rehabil. 2001;23:325–335
- . The contribution of reflex inhibition to arthrogenous muscle weakness. Clin Sci. 1984;67:7–14
- 1 No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated.
- a Kuntovaline Oy, Oltermannintie 8, 00620 Helsinki, Finland.
- b Sammons Preston Rolyan, 4 Sammons Ct, Bolingbrook, IL 60440.
PII: S0003-9993(04)00283-7
doi:10.1016/j.apmr.2003.12.039
© 2004 American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation. Published by Elsevier Inc. All rights reserved.
Volume 85, Issue 10 , Pages 1684-1688, October 2004
