THE INCIDENCE OF FUNCTIONAL disorders of the

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1 1441 ORIGINAL ARTICLE Differences in Isometric Neck Muscle Strength Between Healthy Controls and Women With Chronic Neck Pain: The Use of a Reliable Measurement Barbara Cagnie, PT, PhD, Ann Cools, PT, PhD, Veerle De Loose, PT, Dirk Cambier, PT, PhD, Lieven Danneels, PT, PhD ABSTRACT. Cagnie B, Cools A, De Loose V, Cambier D, Danneels L. Differences in isometric neck muscle strength between healthy controls and women with chronic neck pain: the use of a reliable measurement. Arch Phys Med Rehabil 2007;88: Objectives: To determine the intra- and interrater reliability of the Biodex isokinetic dynamometer to measure the maximal isometric strength of the cervical flexors and extensors, to develop an age- and sex-based normative database in a healthy population, and to evaluate the differences in neck strength between women with chronic neck pain and healthy controls. Design: Cross-sectional. Setting: Physical and rehabilitation medicine department. Participants: Ninety-six healthy volunteers (4 age groups: 20 29, 30 39, 40 49, 50 59y; each consisting of 12 men and 12 women) and 30 women with chronic neck pain. Interventions: Not applicable. Main Outcome Measures: Peak isometric strength of the cervical muscles was tested for flexion and extension by using the Biodex isokinetic dynamometer. The intra- and interrater reliability of the protocol was evaluated in 12 volunteers. Results: The reliability for strength was high for both flexion and extension (intraclass correlation coefficient,.92.96). The mean peak torque for flexion and extension was significantly higher in men (24Nm, 36.4Nm, respectively) compared with women (16.6Nm, 26.5Nm, respectively) (P.001). Peak torque production for extension was significantly lower in the patient group (22.3Nm) compared with the healthy female control group (26.5Nm) (P.003). No significant differences in flexion strength between patient and female control group were found. Conclusions: Results show a high degree of intra- and interrater reliability in measuring isometric neck muscle strength when using the Biodex isokinetic dynamometer. The use of normative data for neck strength when evaluating patients with neck disorders needs to take sex into account. The current study has shown that women with chronic neck pain have lower neck muscle strength in extension than the healthy female group. Key Words: Neck pain; Rehabilitation; Reliability and validity. From the Department of Rehabilitation Sciences and Physiotherapy, Ghent University, Ghent, Belgium (Cagnie, Cools, Cambier, Danneels); and Department of Physical Therapy, Centre for Physical Medicine and Rehabilitation, Queen Astrid Military Hospital, Brussels, Belgium (De Loose). 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. Reprint requests to Barbara Cagnie, PT, PhD, Dept of Rehabilitation Sciences and Physiotherapy, Ghent University Hospital, De Pintelaan 185, 6K3, B-9000 Ghent, barbara.cagnie@ugent.be /07/ $32.00/0 doi: /j.apmr by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation THE INCIDENCE OF FUNCTIONAL disorders of the neck, typically associated with pain and muscular fatigue, is becoming a severe problem in industrial countries, even among young and middle-aged people. 1 It has considerable economic impact through sick leave and an increased use of medication, primary health care services, specialist care, laboratory tests, diagnostic imaging, and therapeutic interventions. 2 There is ample evidence that cervical strength is compromised in various cervical disorders. 2-7 The sustained muscle contraction required to hold the head in various positions and the fatigue caused by muscular weakness are suspected of being contributing factors in chronic neck pain. 2 In women, neck muscle forces are only about half those in men, despite nearly comparable head weights As a consequence, it has been suggested that in women the relatively weak neck muscles cause muscular fatigue syndrome resulting in a higher incidence of chronic neck pain. This emphasizes the need to evaluate strength in women with chronic neck pain. Assessments of cervical strength are useful in the quantification of musculoskeletal impairments and may also be used to provide a basis for assessing the efficacy of therapeutic interventions in patients with neck pain. 11,12 In recent decades, many attempts have been made to obtain an objective method of assessing cervical spine strength. Depending on the study, neck muscle strength in flexion and extension has been measured either with handheld devices 8,13 or devices attached to a solid frame or wall. 9,10,14-16 To successfully distinguish between normal and abnormal strength values in the cervical spine, 2 conditions have to be fulfilled: the derivation of age- and sex-based normative data and high reproducibility of the findings. Different studies 1,8-10,13,15,17 using different test devices have produced divergent results for cervical flexion and extension muscle strength. These discrepancies in normative data highlight the concerns regarding the comparison between different investigations as well as the published normative data and cutoff points between healthy subjects and patients. Because the results of isometric neck strength measurements are highly device dependent, it is necessary to obtain normative data with each type of device used. 12 Second, the positioning of the subjects plays a substantial role in the variation of torque values. 16 In this study, the measurements were taken in the supine position, whereas most of the past studies 1,8-10,13,15,17 were performed with the participants in the seated position. The reliability of measurements using handheld strengthtesting devices is questionable because strength measurements may vary according to the strength of the investigator. 8,13 However, non-handheld isometric neck strength measurement devices specifically built for this purpose seem to have good reliability. 10,14-17 Intraclass correlation coefficients (ICCs) have

2 1442 MUSCLE STRENGTH IN NECK PAIN PATIENTS, Cagnie Fig 1. The strength testing setup for extension. been reported as ranging from.75 to.98 with different test equipment. 10,14-18 However, according to Jordan, 19 the reliability of a tool can only be inferred for the protocol used. This emphasizes the need of determination of reliability and normative data before any differentiation can be made between healthy subjects and patients. The literature is scarce about the relation between chronic neck pain and strength, and there is no consensus in the literature indicating which muscles are affected. Only a few studies 2-4,7,9,10,17 of strength measurements in cervical pathologies have been reported. Researchers 2,9,10,17 have pinpointed both the neck flexor and extensor muscles as sites of weakness, whereas others found significantly lower maximal isometric strength only in the cervical flexor 3,7 or extensor 4 muscles in patients with chronic neck pain. The first aim of this study was to determine the intra- and interrater reliability of the Biodex a isokinetic dynamometer to measure the maximal isometric strength of the cervical flexors and extensors and to develop an age- and sex-based normative database in a healthy population of 96 volunteers. The secondary objective was to evaluate whether women with chronic neck pain had lower neck strength than healthy controls. METHODS Sample Description Ninety-six healthy volunteers and 30 women with chronic neck pain took part in this study. We recruited both healthy subjects and chronic neck pain patients through local advertisement in the hospital. To be included, healthy subjects should not have had neck pain for at least 1 year before testing and should not have been engaged in training of the neck and/or shoulder muscles for at least 6 months before testing. Subjects were asked to fill in a shortened version of the standardized Dutch Musculoskeletal Questionnaire to obtain information about the absence of neck pain during the last year. 20 We divided the healthy subjects into 4 age groups (20 29, 30 39y, 40 49, 50 59y), each consisting of 12 men and 12 women. Subjects were excluded from the study if they had had an operation, were pregnant, had depression or other mental illness, and if they had any specific diseases known to cause chronic neck pain (spinal stenosis, instability or anomaly of the cervical spine, fibromyalgia, inflammatory joint diseases). Written informed consent was obtained from all the volunteers, and the study protocol was approved by the local ethics committee of the Ghent University Hospital. The study design is subdivided into 3 parts, as follows. Intra- and interrater reliability study. Of the 96 healthy volunteers, 12 volunteers (7 men, 5 women) were recruited to participate in the study of intrarater reliability. A total of 12 other healthy subjects (5 men, 7 women) volunteered to take part in the interrater reliability design. One single operator assessed the intrarater reliability, whereas, in the interrater study, 3 other investigators were involved. The investigators consisted of a manual therapist and 2 final-term manual therapy students. The investigators were trained to handle the standardized testing protocol by testing each other and by testing a volunteer not included in the study. Subjects were tested on 3 separate occasions and were scheduled to participate in the study at the same time each day to minimize the possible effects of diurnal changes. The time interval between the 2 tests was consistently 1 week. Normative database. To assess normative data and to determine if isometric cervical musculature strength is sex and age dependent, a descriptive cross-sectional study was performed. Patient study. The results obtained from the neck pain patients were compared with the healthy female data to evaluate whether patients with chronic neck pain have lower neck strength. Because the healthy subjects were tested before the neck pain patients, the raters were not blinded to the status of the subjects. Instrumentation Testing was performed by using a System 3 isokinetic dynamometer. a The isokinetic dynamometer is an electromechanical instrument controlled by a microcomputer, which offers the possibility of objectively and quantitatively evaluating physical parameters of the muscle function such as strength, power, and resistance in different joints during different angular velocities. Experimental Procedure Volunteers were positioned supine for the evaluation of extension and prone for the evaluation of flexion (figs 1, 2). A seat belt was used at shoulder height to prevent any additive strength effect from trunk musculature during the testing procedure. In the supine position, subjects were asked to cross their arms to prevent craniocaudal movements of the thorax. During the experiment, moments were resolved about axes through the midpoint of the line between the C7 spinous process and the sternal notch. Fig 2. The strength testing setup for flexion.

3 MUSCLE STRENGTH IN NECK PAIN PATIENTS, Cagnie 1443 During flexion and extension, the subjects pushed directly forward or backward against the padded strain gauge of the neck strength measurement system. Subjects were verbally encouraged to exert maximal effort. Changing position took about 3 minutes. Three submaximal warmup efforts with gradually increasing force were performed in each direction to acquaint subjects with the testing position and measurement. Subjects were informed initially that to meet the objective of the project it was essential that they exert their maximal effort except in case of onset of any symptoms of pain at which time they were instructed to stop immediately and inform the investigator. Each subject was asked to perform 3 maximal efforts lasting 6 seconds each, starting gradually, building their force to maximum over the first 2 seconds, and then maintaining it over another 4 seconds with a 30-second interval. Measurements were expressed in newton meters. Peak torque was computed, and the mean result of the 3 repetitions was subjected to quantitative comparison and statistical analysis. Statistical Analysis Analysis was performed by using the SPSS statistical software. b Intra- and interrater reliability study. For analysis of intraand interrater reliability, ICCs (2-way mixed-effect model with absolute agreement) 21 with 95% confidence intervals (CIs), standard error (SE) of measurement, and smallest real difference were used. Defined with respect to a 95% level of confidence, the smallest real difference is equal to SE of measurement. Normative database. The results of flexion, extension, and extension and flexion ratios are expressed as means with standard deviations (SDs). Extension and flexion ratios are calculated by dividing the extension values by the flexion values. Two-way analysis of variance with post hoc analysis was used to determine the significance of difference in cervical flexion and extension (dependent variables) for the main factors sex and age (independent variables). An independent samples t test was used to determine the significance of difference in extension and flexion ratio between men and women. Patient study. The normality of variables was evaluated by the Kolmogorov-Smirnov test. Statistical comparison between the groups was performed by using an independent samples t test. P less than.05 was considered statistically significant. RESULTS Descriptive characteristics of the healthy subjects are presented in table 1. The 30 women with chronic neck pain had a Table 1: Anthropometric Data of the Healthy Subjects (n 96) Subjects Age Groups (y) Weight (kg) Height (m) Body Mass Index (kg/m 2 ) Men (n 48) (n 12) (n 12) (n 12) (n 12) Women (n 48) (n 12) (n 12) (n 12) (n 12) NOTE. Values are mean SD. Abbreviation: BMI, body mass index. Table 2: ICC, SE of Measurement (SEM), and Smallest Detectable Difference (SDD) for Intra- and Interrater Neck Strength Measurements Rater Movement ICC (95% CI) SEM SDD Intra Flexion.96 (.91.99) Extension.94 (.85.98) Inter Flexion.92 (.79.98) Extension.94 (.82.98) NOTE. Values are 95% CI. mean age of 32.9 years, a mean height of 166.3cm, and a mean weight of 62.7kg. Intra- and Interrater Reliability Study Interrater reliability and intrarater reliability were analyzed by using the ICC, which varied from.92 to.96, depending on the direction tested (table 2). The SE of measurement ranged from 1.03 to 2.36Nm. Extension yielded higher SE estimates than flexion because of higher maximum strength values. Normative Database The multivariate analysis of variance revealed that peak values were significantly affected by sex in flexion and extension (P.001) but not by age (flexion, P.844; extension, P.408). No significant interaction effect between age and sex was found for flexion (P.122) and extension (P.522). Therefore, normative data were only distributed according to sex (table 3). The average maximum moments resolved at C7-T1 for the men were Nm for extension and Nm for flexion. The maximum moments resolved at C7-T1 for the women were Nm for extension and Nm for flexion. The mean extension and flexion ratios were for men and for women. When comparing the strength of men and women, men proved to be 40% stronger for flexion (P.001) and 44% for extension (P.001). No significant differences between men and women were found when comparing extension and flexion ratio (P.685). Patient Study When comparing the strength between the healthy subjects and the female neck pain patients, only the female healthy group (n 48) was selected because there was a significant difference in strength between men and women. The peak torque production for extension and extension and flexion strength ratios were significantly lower in the patient group compared with the female healthy control group (table 4). No Table 3: Mean Isometric Neck Muscle Strength in Flexion and Extension by Sex and Age Subjects Age Group (y) Flexion Extension Men (n 48) (n 12) (n 12) (n 12) (n 12) Women (n 48) (n 12) (n 12) (n 12) (n 12) NOTE. Values are mean newton meters SD.

4 1444 MUSCLE STRENGTH IN NECK PAIN PATIENTS, Cagnie Table 4: Peak Neck Strength Values in Women With Chronic Neck Pain and Healthy Female Controls Movement Healthy Women (n 48) Neck Pain (n 30) Flexion (Nm) Extension (Nm) Extension/flexion ratio NOTE. Values are mean newton meters SD. significant difference emerged in the flexion strength between the patient and female control group. DISCUSSION A considerable number of reliability and validity studies 11,15-17 examining cervical strength have been identified in the literature, and, from this point of view, the present study cannot claim novelty. The strength of this study is that the results of the neck patient group are preceded by a reliability study and determination of a normative database. Discrepancies exist among similar studies 1,8-10,13,15,17 regarding normative data, which highlights the concerns regarding the comparison between different investigations as well as the published normative data and cutoff points between healthy subjects and patients. This emphasizes the need of determination of reliability and normative data before any differentiation can be made between healthy subjects and patients. We chose to measure neck strength isometrically because the major physiologic function of the neck muscles is to stabilize the neck and carry the head (postural muscles), an isometric function. However, isometric neck strength cannot be considered as a direct estimation of functional ability, which by nature is complex and influenced by several factors, such as neuromuscular function and range of motion. 15 Intra- and Interrater Reliability Study The results of the present study show high intra- and interrater reliability in cervical isometric strength measurement when using the Biodex isokinetic dynamometer. The mean ICCs calculated were at least.92. It would, therefore, appear that the methodology reported here is reliable and robust for such studies. These results are comparable to previous studies 10,14-18 in which ICC values ranged from.76 to.98. Normative Database Knowledge of normative values for cervical muscles is essential for the design and execution of rehabilitation programs. The average maximum moments resolved at C7-T1 for the men were 36.4Nm for extension and 24Nm for flexion. The maximum moments resolved at C7-T1 for the women were 26.5Nm for extension and 16.6Nm for flexion. Comparison with previous neck strength studies in which moments were expressed as newton meters revealed that in men flexion ranged from 17 to 30Nm and extension from 42 to 60Nm. In women, flexion varied from 11 to 21Nm and extension from 21 to 48Nm. 9,10,15,22 This variation in the torque values across different studies 16,23 in the literature could possibly be caused by the equipment and technique used, positioning of subjects, training effect, or ethnic differences. Although the Biodex isokinetic dynamometer is frequently used in practice and research to evaluate physical parameters of muscle function, as far as we know, it has not been used in previous studies for the measurement of cervical strength, except for the study by Seng et al. 18 The measurements were undertaken with the participants in the supine P position, although most of the studies were undertaken with the participants in the seated position. Peolsson et al 15 observed that strength in extension in the sitting position was twice as high as that previously reported in the prone position. This may explain why our results were slightly lower than most of the other results found in the literature. However, we are aware that it is more natural to test and train muscles in the positions of their use during daily activities. Differences in age. No significant difference was found in muscle strength with different age groups. These results show that the subjects in this study were able to maintain a good level of isometric neck muscle strength in all directions until their sixth decade. These findings correlate with most of the studies found in the literature, 8-10 although some others reported an age-related decrease in neck strength. 15 It is accepted generally that skeletal muscle strength increases take place until approximately the age of 30 years followed by a period of strength maintenance until age 50 or 60 years; at this time, strength begins to decline as muscle mass decreases. 10 Because the maximum age of our studied population was 59, this could explain why no age effect was found. Second, the small sample size may represent a limitation of the data. However, Salo et al 12 evaluated a larger number of participants in a recent study (220 women divided into 4 age groups), but he also did not find a statistically significant difference in neck strength among the different age groups. Differences in sex. The men exhibited superior maximal isometric strength levels in both the flexors and the extensors of the cervical spine as compared with the women. When comparing the strength of men and women, men proved to be 40% stronger for flexion and 44% for extension. This is in accordance with the literature in which male-to-female strength values ranged from 1.2 to 2.5, 9,10,22 with a mean range from 1.7 to ,15 This strength difference corresponds well with that of other studies regarding spinal musculature. 10 Differences in maximum moments between men and women may arise from differences in posture, muscle size, or neural activation. Extension/flexion ratio. Mean extension/flexion ratio was 1.56 for men and 1.50 for women. The larger extension strength over flexion by 50% reflects the postural role of extensor musculature and obvious muscle mass difference between posterior and anterior muscles of the cervical spine. This association between the extensors and flexors of the cervical spine was found to be similar to the range of lumbar spine. 10 An explanation for this may be that the center of gravity of the head during activity, such as reading, is often located in front of the axis of rotation, leading to higher postural demands on the neck extensor muscles. Another explanation could be that the extensor muscles situated posterior to the line of rotation of the cervical spine have a longer lever arm and thereby a mechanical advantage over the flexor muscles. 15 There were no significant differences in ratio between men and women, although most of the previous studies, 10 except Peolsson s study, 15 showed that women are proportionately stronger in extension and/or proportionately weaker in the flexion as compared with men. Patient study. Peak isometric neck strength values were statistically significantly reduced in the women with chronic neck pain compared with female healthy controls in extension and extension and flexion ratio but not in flexion. A number of studies have reported that the patient populations had significantly less muscle strength than the control populations, but a consensus regarding the muscles that are affected is lacking. Researchers 2,9,10,17 have pinpointed both the neck flexor and extensor muscles as a site of weakness. Prushansky et al 4 found significantly lower maximal isometric strength of the cervical extensor muscles in patients with chronic neck pain compared with

5 MUSCLE STRENGTH IN NECK PAIN PATIENTS, Cagnie 1445 healthy matched controls, whereas Silverman et al 3 and Barton and Hayes 7 found that isometric flexion strength in patients with chronic neck pain was about 50% of that of healthy controls. It could be argued that the presence of persistent neck pain may cause patients to avoid daily activities, which may lead to specific physical deconditioning (eg, loss of strength and endurance of paraspinal muscles). This may result in even more pain and disability and so contribute to the chronicity of neck pain. 24 According to Ylinen et al, 6 part of the difference may be explained by neural inhibition caused by pain felt during test efforts, which does not normally cause any pain. A lower pressure pain threshold referring to local allodynia has been shown in patients with neck pain, which may prevent patients from producing full force because of conscious or subconscious fear of hurting themselves. Most of the pain in chronic neck pain patients is situated posteriorly, which may explain the lower extension/flexion ratio. 4 CONCLUSIONS Results show a high degree of intra- and interrater reliability in measuring isometric neck muscle strength. Establishing valid and reliable measures of neck function will enable clinicians to monitor intervention effects over time within groups of patients. The use of normative data for neck strength when evaluating patients with neck disorders needs to take gender into account. The current study has shown that women with chronic neck pain have lower neck muscle strength in extension than the healthy female group. Knowledge of the reduction in neck strength is essential in planning individually tailored neck strength training programs. References 1. Garcés G, Medina D, Milutinovic L, Garavote P, Guerado E. Normative database of isometric cervical strength in a healthy population. 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J Manipulative Physiol Ther 2000;23: Cagnie B, Danneels L, Van Tiggelen D, De Loose V, Cambier D. Individual and work related risk factors for neck pain among office workers: a cross sectional study. Eur Spine J 2007;16: Shrout P, Fleiss J. Intraclass correlations: uses in assessing rater reliability. Psychol Bull 1979;86: Vasavada A, Li S, Delp S. Three-dimensional isometric strength of neck muscles in humans. Spine 2001;26: Suryanarayana L, Kumar S. Quantification of isometric cervical strength at different ranges of flexion and extension. Clin Biomech (Bristol, Avon) 2005;20: Smeets R, Wade D, Hidding A, Van Leeuwen P, Vlaeyen J, Knottnerus J. The association of physical deconditioning and chronic low back pain: a hypothesis-oriented systematic review. Disabil Rehabil 2006;28: Suppliers a. System 3; Biodex Medical Systems Inc, 20 Ramsay Rd, Shirley, NY b. Version 11; SSPS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL