- Email: [email protected]
Differences in Cervical Multifidus Muscle Thickness During Isometric Contraction of Shoulder Muscles: A Comparison Between Patients With Chronic Neck Pain and Healthy Controls
DIFFERENCES IN CERVICAL MULTIFIDUS MUSCLE THICKNESS DURING ISOMETRIC CONTRACTION OF SHOULDER MUSCLES: A COMPARISON BETWEEN PATIENTS WITH CHRONIC NECK PAIN AND HEALTHY CONTROLS Leila Rahnama, PT, PhD, a Asghar Rezasoltani, PhD, b Minoo Khalkhali Zavieh, PhD, c
Farhang NooriKochi, MD, d and Alireza Akbarzadeh Baghban, PhD e
ABSTRACT Objective: The purposes of this study were to (1) measure the thickness of cervical multifidus muscle (CMM) in different maximal voluntary contraction percentages of isometric contraction of shoulder muscles, (2) evaluate the differences of the CMM thickness in different directions of the shoulder movement, and (3) compare the changes in the CMM thickness of participants with neck pain and also of healthy individuals. Methods: Twenty healthy men (age, 27.45 ± 4.37 years; height, 177 ± 4.66 cm; weight, 72.85 ± 6.46 kg) and 20 men with chronic mechanical neck pain (age, 28.90 ± 5.53 years; height, 176 ± 5.98 cm; weight, 73.15 ± 7.82 kg) participated in the study. Both the right and left CMM thicknesses were measured using an ultrasound device while participants performed isometric contraction of shoulder muscles in 6 movement directions. Results: In both groups, an increment of CMM thickness followed as the increase of isometric force (P b .01).The increase of muscle thickness of healthy participants was substantially more than the chronic mechanical neck pain participants (P = .03). Although no significant difference of CMM thickness was seen among the effects of the 6 force directions (P N .05), there was a significant difference of activity noted between the left and right sides (P = .047). Conclusion: The results of the present study indicate that isometric contraction of shoulder muscles caused an increase in the CMM thickness regardless of force direction. This increase was seen in both groups of healthy participants and patients with neck pain. However, less thickness changes were observed in participants with neck pain, which may be interpreted as reduced CMM activity in such people. (J Manipulative Physiol Ther 2015;38:210-217) Key Indexing Terms: Ultrasonography; Neck Muscle; Neck Pain; Isometric Contraction; Muscle Size; Shoulder
articipants with chronic neck pain have altered neck muscle activities compared with healthy participants. 1–4 Proprioceptive deficit, sensorimotor disturbances, 5 reduced neck muscle strength, and endurance 6,7 are general
P a
Assistant Professor of Physiotherapy, Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran. b Professor of Physiotherapy, Faculty of Rehabilitation, Physiotherapy Research Center, Shahid Behesht University of Medical Sciences, Tehran, Iran. c Assistant Professor of Physiotherapy, Faculty of Rehabilitation, Department of Physiotherapy, Shahid Behesht University of Medical Sciences, Tehran, Iran. d Radiologist, Specialist Doctor, Department of Radiology, Medical Imaging Research Center, Shiraz University of Medical sciences, Shiraz, Iran.
manifestations of chronic neck pain. Recently, atrophic changes and reduced deep cervical muscles size and thickness have been reported in these participants. 8,9 Because deep dorsal neck muscles including the cervical multifidus muscle e
Associate Professor of Biostatistics, Faculty of Rehabilitation, Department of Basic Sciences, Shahid Behesht University of Medical Sciences, Tehran, Iran. Submit requests for reprints to: Leila Rahnama, PT, PhD, Assistant Professor of Physiotherapy, Deprtment of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran. (e-mail: [email protected] [email protected]). Paper submitted May 16, 2013; in revised form November 6, 2014; accepted November 10, 2014. 0161-4754 Copyright © 2015 by National University of Health Sciences. http://dx.doi.org/10.1016/j.jmpt.2014.11.008
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(CMM) have been shown to play a role in providing neck stability and preventing strains to cervical structures, 10,11 strengthening them is of prime concern while treating patients. Several studies have shown that physical exercises might facilitate increase in muscle strength and improve muscle activity. 4,12–15 However, these studies focused on general training of neck muscles rather than exercises for a selected muscle like CMM. 15,16 Therefore, there is still a need to further expand knowledge concerning activities for each neck muscle. Some studies have targeted areas of the neck. Lee et al 17 reported changes in CMM thickness as an effect of isometric head extension at different levels of the cervical spine in healthy participants. Peolsson et al 18 measured the different activity patterns of cervical muscles, especially for the CMM, during a loaded arm lifting task between healthy participants and patients with long-standing neck pain. What these studies did not investigate, however, is the behavior of the CMM contraction and how it responds to different amounts of force exerted by the shoulder muscles and also the different movement directions of the upper extremities. Various methods are used to investigate neck muscles functions, such as magnetic resonance imaging and ultrasound imaging. 18–20 Among these, ultrasound imaging is recognized as a reliable and valid method of muscle function evaluation in real time. 9,21–23 In recent research studies, the interest in ultrasonography measurement of muscle dimensions has greatly increased. For instance, some studies reported dimensions of the CMM at rest or during an isometric head extension as an index for muscle activity using ultrasound. 8,17,24 However, it is unknown whether the CMM dimensions change during a task involving the upper extremities of patients with chronic neck pain. Further studies are required to reveal this little known aspect of neck muscles functions. We hypothesized that the CMM thickness will change during an isometric contraction of the shoulder muscles in different movement directions in healthy participants more than that of participants with neck pain. Therefore, the purposes of this study were to (1) measure the thickness of CMM in different maximal voluntary contraction (MVC) percentages of isometric contraction of shoulder muscles, (2) evaluate the differences of the CMM thickness in different directions of the shoulder movement, and (3) compare the changes in the CMM thickness of participants with neck pain and also of healthy individuals.
METHODS Participants Twenty participants with chronic mechanical neck pain (CMNP) and 20 healthy individuals voluntarily participated in the study. Participants were recruited from bank office workers. A total of 300 questionnaires containing the study
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Fig 1. Inclusion and exclusion criteria for participants of the study. criteria were distributed among them. Then, the researcher collected the questionnaires and announced those who met the eligibility criteria and stated that they agree to participate in the study. Participants were all male and at least 18 years old with no regular gym activity. The general eligibility criteria include having no any history of trauma or surgery on the spine, any congenital or inflammatory diseases, or shoulder and arm pain. The inclusion and exclusion criteria for participants are listed in Figure 1. Participants in both groups were comparable in terms of age, weight, height, and body mass index (BMI). The procedure was explained to the participants, and they signed the informed consent forms prior to the study. This study was approved by the Research Ethics Board of the Faculty of Rehabilitation, Shahid Beheshti University of Medical Sciences.
Ultrasonography Measurements Ultrasonographic imaging of the CMM was conducted by an ultrasonography device (Accuvix V20 prestige; Samsung, Medison, Korea) with a 8-MHz, 4 .5-cm linear array transducer. An experienced physical therapist identified the spinous process of C4 by palpation. Further clarification was carried out with the help of ultrasonography. We evaluated the CMM at the level of C4, as it has been reported to have a greater cross-sectional area (CSA) than C3 and the same CSA as C5 and C6. 8 Lee et al 23 also investigated the thickness of CMM at the level of C4. At that point, the examiner placed the transducer transversely at the level of the C4 spinous process, moving it slowly to the right or left side and slightly upward and downward so as to identify the echogenic vertebral lamina clearly. At this level, the CMM was located laterally to the spinous process, rotator muscle, and laminar junction;
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Fig 2. Ultrasonographic image of CMM at level C4. medially to the articular process; and just below the fascia of the semispinalis cervicis muscle. 17 The distance from the echogenic vertebral lamina to the interfacing fascia of semispinalis cervicis muscle was measured from border to border at the widest distance as the anterior-posterior dimension (APD) or the thickness of the CMM. The images were taken firstly while the participants were at rest and then with applied force to reach their MVCs of the right shoulder muscles in 6 movement directions (Fig 2).
Muscle Strength The shoulder muscles strength was recorded by a load cell model H3-C3-100 Kg-3B (ZEMIC, Shaanxi, China). The load cell was positioned on a U-shaped groove installed on an arm rest and fixed onto the right side of a custom-made chair so the participants could put their right forearms on it. The groove was designed in a way that allowed the load cell to move in order to record the forces in 6 directions of shoulder movements (flexion, extension, external rotation, internal rotation, abduction, and adduction). The participants were then asked to perform isometric contraction of the shoulder muscles in 6 desired directions and gradually reach their MVCs.
Experimental Procedure Participants were seated relaxed on a chair while keeping their heads and necks in a neutral position and their dominant (right) forearms laid on the armrest. Two thorax and pelvic belts were used to secure participants in the chair (Fig 3). The belts were fastened at the level of the scapular spine and iliac crest, respectively. Then the procedure was completely explained to the participants, and they were asked to perform 3 trial runs of randomly chosen directions to make sure that they were acquainted with the procedure. To start the experimental procedure, the participants were asked to push their right forearms onto the loadcell and
Fig 3. The position of participants during the experimental procedure. (Color version of figure is available online.)
increase their force gradually to reach their MVCs in 10 seconds. Three trials in each force direction were performed with 1-minute intervals between each trial. Then after a 2-minute interval, the next force direction was applied. After completing the procedure in all 6 directions, the participants were given a 15-minute rest before repeating the actions conducive to the evaluation of the effects of isometric contraction of the right shoulder muscles on the left CMM. The trials with maximum force in each direction were selected for data analysis. Then the amount of identical force for 25%, 50%, 75%, and 100% of MVC were identified by a custom-made software for later analysis.
Sonosynch Software A custom-designed software with a sampling rate of 20 per second was used to pick up and store the load cell data and ultrasound images in a synchronized way to enable the examiner to analyze the data offline. The software could pick out and store 20 force data and 20 identical ultrasound images in a second. Therefore, the examiner was provided with forces which ranged from 0 to 100% MVCs and their identical images for data analysis. The distance from the echogenic vertebral lamina to the interfacing fascia of semispinalis cervicis muscle was measured border to border at the widest distance, as was the anterior-posterior dimension or the thickness of CMM.
Reliability Study For the examiner to assess the repeatability of the right CMM thickness measurement at rest and 100% MVC
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Table 1. Comparison of MVC of Shoulder Muscles in Newton (N; Mean ± SD) in 6 Movement Directions of the Shoulder Joint Between the 2 Groups Abduction Adduction Flexion Extension External rotation Internal rotation
Healthy
Participants With CMNP
P
14.91 ± 3.67 14.57 ± 5.71 14.37 ± 6.44 10.93 ± 3.48 10.54 ± 2.30 14.25 ± 4.85
14.01 ± 4.11 14.03 ± 5.28 12.08 ± 4.25 10.30 ± 2.52 10.68 ± 3.51 12.86 ± 4.22
.48 .76 .19 .52 .88 .34
CMNP, chronic mechanical neck pain.
and the maximum strength of the shoulder muscles, the intratester reliability was carried out on both groups, obtaining the data collected on 2 separate occasions of which were collected 3 to 7 days apart. A total number of 24 participants were included (12 healthy and 12 participant with neck pain).
Statistical Analysis The statistical analysis was performed with SPSS software (version 16; SPSS Inc, Chicago, IL). An Independent t test was used to compare the participants' anthropometric data and the isometric force of shoulder muscles between the 2 groups. To assess the reliability of the muscle thickness measurement and the shoulder muscle force, intraclass correlation coefficient (ICC) was used to determine relative reliability and the SEM, and the smallest detectable difference (SDD) were used to determine absolute reliability. The Bland and Altman plot was used to determine the measurements agreement on 2 occasions. The mean differences of measurements on 2 occasions were organized as a reference line on a y axis and ± 1.96 times the SD as limits of agreement. A multifactorial analysis of variance for repeated measures with force (0, 25%, 50%, 75%, and 100% MVC), direction (6 movement directions of the shoulder joint), and side (the right and left CMM) as 3 within factors and group (participants with CMNP and healthy controls) as the between factor was used to evaluate changes in the CMM thickness. The assumption of sphericity has not been met. An α of .05 was taken as the level of significance.
RESULTS Twenty participants with CMNP (age, 28.90 ± 5.53 years; height, 176 ± 5.98 cm; weight, 73.15 ± 7.82 kg; BMI, 23.44 ± 1.59 kg/m 2) and 20 healthy individuals (age, 27.45 ± 4.37 years; height, 177 ± 4.66 cm; weight, 72.85 ± 6.46 kg; BMI, 23.28 ± 1.67 kg/m 2) participated in the present study. The independent t test showed no significant difference in age (P = .36), height (P = .81), weight (P = .81), and BMI (P = .75) between the 2 groups.
Fig 4. a, Bland-Altman plot for cervical multifidus thickness at rest measured in 2 separated days for healthy participants. b, Bland-Altman plot for cervical multifidus thickness at rest measured in 2 separated days for participants with CMNP. The independent t test revealed no significant difference for maximum isometric strength of shoulder muscles in none of the 6 directions between the 2 groups (Table 1). The intratester reliability of the right CMM thickness measurement at rest was high in both groups, with ICC of 0.89 and 0.84, SEM of 0.05 and 0.04, and SDD of 0.14 and 0.11 in healthy participants and participants with CMNP, respectively. As for the reliability of the right CMM thickness measurement at 100% MVC in 6 movement directions in both groups, the reliability was also high, with an ICC ranging from 0.75 to 0.90, SEM ranging from 0.04 to 0.06, and SDD ranging from 0.11 to 0.17. Similarly, the reliability of the maximum muscles strength at 100% MVC of shoulder muscles in all directions was high, with ICC ranging from 0.75 to 0.99, SEM ranging from 0.63 to 2.10, and SDD ranging from 1.74 to 5.82. The agreement between the measurements for CMM thickness at rest on 2 occasions is demonstrated in Figure 4a for healthy participants and in Figure 4b for participants with
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Table 2. Mean and SD for Anterior-Posterior Dimension of CMM in Healthy Participants and Participants With Neck Pain Direction Side
MVC %
Healthy participants Right 0 25 50 75 100 Left 0 25 50 75 100 Participants with neck pain Right 0 25 50 75 100 Left 0 25 50 75 100
Abduction
Adduction
Extension
Flexion
External Rotation
Internal Rotation
1.09 ± 0.17 1.15 ± 0.15 1.15 ± 0.15 1.15 ± 0.15 1.17 ± 0.21 1.07 ± 0.15 1.12 ± 0.15 1.12 ± 0.15 1.12 ± 0.15 1.14 ± 0.15
1.09 ± 0.17 1.10 ± 0.16 1.11 ± 0.16 1.12 ± 0.17 1.13 ± 0.17 1.07 ± 0.15 1.09 ± 0.16 1.10 ± 0.16 1.10 ± 0.18 1.11 ± 0.15
1.09 ± 0.17 1.12 ± 0.17 1.10 ± 0.17 1.14 ± 0.15 1.15 ± 0.16 1.07 ± 0.15 1.12 ± 0.15 1.12 ± 0.15 1.12 ± 0.16 1.14 ± 0.18
1.09 ± 0.17 1.11 ± 0.17 1.13 ± 0.17 1.13 ± 0.17 1.15 ± 0.14 1.07 ± 0.15 1.09 ± 0.12 1.10 ± 0.14 1.08 ± 0.12 1.11 ± 0.12
1.09 ± 0.17 1.13 ± 0.15 1.15 ± 0.14 1.16 ± 0.14 1.17 ± 0.14 1.07 ± 0.15 1.08 ± 0.18 1.08 ± 0.18 1.08 ± 0.19 1.11 ± 0.18
1.09 ± 0.17 1.11 ± 0.15 1.13 ± 0.17 1.13 ± 0.18 1.13 ± 0.16 1.07 ± 0.15 1.11 ± 0.14 1.09 ± 0.15 1.08 ± 0.16 1.12 ± 0.18
1.13 ± 0.16 1.16 ± 0.16 1.15 ± 0.18 1.18 ± 0.15 1.16 ± 0.16 1.09 ± 0.17 1.09 ± 0.13 1.10 ± 0.14 1.08 ± 0.14 1.11 ± 0.15
1.13 ± 0.16 1.15 ± 0.16 1.15 ± 0.17 1.15 ± 0.16 1.17 ± 0.17 1.09 ± 0.17 1.14 ± 0.16 1.12 ± 0.17 1.10 ± 0.17 1.13 ± 0.14
1.13 ± 0.16 1.13 ± 0.17 1.14 ± 0.16 1.16 ± 0.16 1.17 ± 0.16 1.09 ± 0.17 1.09 ± 0.11 1.10 ± 0.12 1.11 ± 0.15 1.11 ± 0.16
1.13 ± 0.16 1.13 ± 0.16 1.14 ± 0.18 1.15 ± 0.16 1.13 ± 0.17 1.09 ± 0.17 1.12 ± 0.15 1.12 ± 0.16 1.11 ± 0.15 1.10 ± 0.14
1.13 ± 0.16 1.12 ± 0.15 1.16 ± 0.16 1.17 ± 0.18 1.15 ± 0.19 1.09 ± 0.17 1.10 ± 0.17 1.08 ± 0.18 1.09 ± 0.18 1.10 ± 0.16
1.13 ± 0.16 1.16 ± 0.15 1.15 ± 0.16 1.15 ± 0.16 1.16 ± 0.14 1.09 ± 0.17 1.12 ± 0.13 1.11 ± 0.14 1.13 ± 0.13 1.13 ± 0.15
%MVC, percent of maximum voluntary contraction.
CMNP. The mean differences were − 0.005 with 95% confidence interval of − 0.195 to 0.185 cm and 0.0005 with 95% confidence interval of − 0.1545 to 0.1555 cm for healthy participants and participants with CMNP, respectively, indicating an acceptable to good levels of agreement between the 2 measurements. The CMM thickness was not significantly different at the baseline between the 2 groups. The mean and SD of the CMM thickness in both groups are presented in Table 2. The mean and SD of the visual analog scale and the neck disability index (NDI) were 4.9 ± 1.8 and 13.4% ± 5.95%, respectively, in the group of chronic pain participants. The results of our study have shown that there was a significant main effect of force on the CMM thickness (F1.47,55.78 = 13.72, P b .001). It demonstrated an increased thickness as the shoulder muscles' strength increased to reach 100% MVC. The main effect of each side was also statistically significant (F1,38 = 4.23, P = .047), indicating that the CMM thickness on the right side underwent more changes compared with the left side. The interaction of group by force was significant (F1.47,55.78 = 2.81, P = .027), indicating a more considerable increase in the CMM thickness during isometric contraction of the shoulder muscles in healthy participants than in participants with CMNP. No other main or interaction effects for CMM thickness were significant for a group (F1,38 = 0.12, P = .73), direction (F3.81,144.97 = 0.43, P = .83), group by direction (F3.81, 144.97 = 1.30, P = .26), direction by force (F10.34, 392.87 = 0.67, P = .86), side by direction (F5,190 = 1.42, P = .22), side by force (F1.50,57.14 = 0.71, P = .59), group by force by direction
(F10.34,392.87, P = .15), group by direction by side (F4.31,163.78, P = .76), side by direction by force (F10.53,400.23 = 1.02, P = .43), force by side by group (F1.50,57.14 = 0.08, P = .99), and force by group by direction by side (F10.53,400.23 = 0.72, P = .81).
DISCUSSION We found out that CMM thickness increased while isometric force of the shoulder muscles increased. This finding is seen in both groups. A possible underlying mechanism for this finding is that the CMM is a cervical stabilizer, 24 so it is possibly contracted during performance of tasks by the upper extremities to stabilize the cervical spine. Such findings have been previously reported for the lumbar multifidus muscle. Danneels et al 25 reported an increase in the CSA of the lumbar multifidus muscle after a period of resistive training of the lower extremities. This finding is consistent with previous reports that the deep neck extensor muscles including CMM are activated during a lifting task to support the cervical spine. 18 A novel aspect of this study was evaluating differences of the thickness of CMM during isometric contraction of the shoulder muscles between participants with CMNP and healthy controls. According to our results, the interaction of force by group was significant for the CMM thickness. It implies that isometric contraction of shoulder muscles led to different changes in the CMM thickness in participants with neck pain and healthy participants regardless of the force direction and the side of CMM. We found that an increase
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in force production by the shoulder muscles led to an increase in the CMM thickness, although in healthy participants, the muscle thickness increased more considerably than that in participants with neck pain. This observed difference between the 2 groups may be because participants with neck pain confront a lot of physiological changes such as a weakness of deep muscles, 1,9,26 prompting their inability to activate their CMM as much as healthy individuals. A further problem associated with CMNP is the presence of active trigger points in the deep extensor muscles of participants with CMNP, which may cause restriction of the deep extensor muscles activation in such a population. 27 Our results also support those of Cagnie et al, 28 who showed a reduced activity of the CMM during a cervical extension task in an experimentally pain-induced condition when compared with a no-pain condition. However, our results are not in line with the results of the study conducted by Peolsson et al, 18 who found a greater deformation rate of the CMM during a loaded arm lifting task in participants with long-standing pain than in healthy individuals. Because it was demonstrated that there is a linear correlation between the degree of muscle contraction and the corresponding degree of muscle deformation, we can conclude that the greater muscle deformation rate in participants underwent anterior cervical decompression and fusion in the study by Peolsson et al indicates a higher muscle contraction in such participants. Our findings do not support this either. A different population undergoing the study or a different evaluation method of the muscle function might explain the discrepancy of the results. Findings by Peolsson et al 18 are notable due to illustration of an altered behavior in deep neck muscles of participants with long-standing neck pain. This implies altered motor strategies to support the cervical spine in such participants. Alternatively, Sheard et al 19 found altered activity and length-tension relations of the trapezius and the levator scapula in patients with neck pain. 20 These muscles have expanded attachments to the cervical spine, making the cervical vertebrae rotate during tasks performed by the upper extremities. 29 As a result, their altered length-tension relations may affect the amount and the nature of the vertebral motions. This may lead to an altered function of deep neck muscles like the CMM, aiming to stabilize the cervical spine in participants with neck pain. This study demonstrated that the mean thickness of the CMM on the right side was statistically larger than that of the left side at the level of C4. This might be because all participants in the present study were right handed. This finding is not in agreement with that of Fernández-de-las-Peñas et al, 8 who reported no statistically significant difference between the CSA of CMM on the 2 sides. However, their reported CSA of CMM on the right side was greater than the left one. Rankin et al 30 have also reported the symmetry of CMM between the 2 sides. The disagreement between the results could be because we measured the thickness of CMM while researchers of previous studies measured the CSA of CMM, which had been affected by muscle thickness and other dimensions of the muscle.
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The main effect of direction was not significant, concluding that the isometric contraction of shoulder muscles in all 6 directions had the same effect on the CMM thickness. These results are expectable because it has been claimed that the multifidus muscle provides the stability of the spine regardless of the direction of movement. 31 No statistically significant baseline difference in the thickness of CMM was seen in participants with CMNP when compared with healthy people. This result does not support the findings of Kristjansson, 22 who showed a reduced thickness of CMM in participants with neck pain. This discrepancy of the result may be due to the different group of participants involved in the study. Kristjansson evaluated people with chronic whiplash-associated disorder, whereas our participants had experienced neck pain for 3 months in the last year. Some have argued that neck pain may cause muscle atrophy via reflex. 32 Although this short period of pain experienced by our tested participants may not be long enough to change the muscle, patients participating in the study by Kristjansson et al had a higher disability index than did our participants and a higher age range. This is justifiable because the greater the duration of neck pain, the greater NDI and probably more atrophy in muscles. 8 Fernández-de-las-Peñas et al also found a smaller CSA in patients with neck pain compared with healthy people. This is not in agreement with our study, as participants in their study had a mean NDI of 27.6, whereas our participants had the mean NDI of 13.6, almost half the patients studied by Fernández-de-las-Peñas et al. 8 The isometric forces of shoulder muscles in 6 movement directions in participants with neck pain were not significantly different with healthy individuals. This result was expectable as participants with CMNP had no pain or discomfort in their shoulder area. Therefore, the isometric strength of their shoulder muscles was equal to their healthy controls. Similarly, Peolsson et al 33 found no significant difference in neck muscle strength during an isometric contraction of neck muscles between healthy participants and participants with long-standing neck pain. However, they argued at the small size of the examined population and on the large interindividual differences as possible cause of such similarities. Both arguments are not applicable to our case study. Our results do not support the findings presented by Osborn and Jull 34 where it shows that neck pain is in association with upper limb disability. They reported a moderate to high relationship between the NDI and upper limb disability. Our results are reasonable as the participants in their study had a mean NDI of 27.7, whereas our participants had the mean NDI of 13.4, which is almost half the NDI of those participants. We saw no difference in the shoulder muscle strengths between the 2 groups. Some activities reported as to be difficult or to be disturbing to participants in aforementioned study were those needing the neck to be extended or flexed, such as overhead activities and gardening, whereas participants in our study kept their neck in a neutral position during the
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experimental procedure. This enabled them to do the isometric task of shoulder muscles with no induced pain or restriction. Osborn and Jull presented that patients with neck and arm pain demonstrated more upper limb disability than participants with neck pain only. It is notable that our participant population had no arm or shoulder pain. Our findings do not support the results of the study by McLean et al 35 demonstrating upper limb disability in patients with neck pain. The mostly high level of disability (mean Northwick Park Neck Pain Questionnaire of 38.7) in patients participating in their study may explain the reason for the different findings. We also evaluated the intraexaminer reliability in measuring the CMM thickness to assess the accuracy of the results. Our results also showed that the intraexaminer reliability of measuring the CMM thickness was high both at rest and during contraction in healthy participants and patients with neck pain. Similar reports of the reliability for CMM ultrasonography have already been reported. 22 Lee et al 23 also reported ultrasonography measurement of the thickness of CMM by an examiner as a reliable and valid method to evaluate CMM function.
LIMITATIONS Male participants were only considered in the present study. It is recommended to compare current results with deep neck muscles behavior in women. Another limitation is that the isometric task did not resemble functional tasks and did not represent normal function of neck muscles. Future studies may be needed to compare the activity of CMM in response to daily tasks in both men and women. The results of this study cannot be generalized to all participants with neck pain, as we only evaluated participants with CMNP and an average visual analog scale score of 4.9. To permit a more generalized interpretation, a population-based epidemiologic study is needed. The case-control design of the study did not allow us to evaluate the training effect of isometric contraction of shoulder muscles on CMM thickness; future clinical trials should address this issue. Further studies may also be required to determine the effect of hand dominancy on the size of CMM. Finally, the sitting position of our participants in the present study was a comfortable condition, letting them focus on their shoulders isometric forces. Evaluating the CMM responses to a task of the upper extremities during a more challenging position like standing may shed more light on the stabilizer role of the CMM, when it has to send more afferent information to the brain affecting postural stability. 36
CONCLUSION The results of the present study suggest that isometric contraction of shoulder muscles causes an increase in the CMM thickness regardless of force direction. This increase was seen in both groups of healthy participants and patients with neck pain. However, less thickness changes were
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observed in participants with neck pain, which may be interpreted as reduced CMM activity in such people.
Practical Applications • The CMM thickness increased during the isometric contraction of shoulder muscles in all 6 directions of shoulder movements. • The changes in CMM thickness were seen both in healthy participants and people with chronic neck pain. • The CMM thickness increased while the isometric contraction of shoulder muscles increased to reach 100% MVC. • Patients with chronic neck pain showed lesser changes in CMM thickness compared with healthy individuals.
ACKNOWLEDGMENT We thank the manager of Marvdasht Physiotherapy Clinic, Ms Manizheh Saberi, PT, for her assistance in enrolling and screening the participants of the study.
FUNDING SOURCES AND POTENTIAL CONFLICTS OF INTEREST No funding sources or conflicts of interest were reported for this study.
CONTRIBUTORSHIP INFORMATION Concept development (provided idea for the research): A.R., and L.R. Design (planned the methods to generate the results): L.R., and A.R. Supervision (provided oversight, responsible for organization and implementation, writing of the manuscript): A.R., and M.K.h. Data collection/processing (responsible for experiments, patient management, organization, or reporting data): L.R., and F.N. Analysis/interpretation (responsible for statistical analysis, evaluation, and presentation of the results): L.R., and A.A. Literature search (performed the literature search): L.R. Writing (responsible for writing a substantive part of the manuscript): L.R. Critical review (revised manuscript for intellectual content, this does not relate to spelling and grammar checking): L.R., A.R., M.K.h., and F.N.
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REFERENCES 1. Falla D, Bilenkij G, Jull G. Patients with chronic neck pain demonstrate altered patterns of muscle activation during performance of a functional upper limb task. Spine 2004;29: 1436-40. 2. Falla D, O'Leary S, Fagan A, Jull G. Recruitment of the deep cervical flexor muscles during a postural-correction exercise performed in sitting. Man Ther 2007;12:139-43. 3. Johnston V, Jull G, Souvlis T, Jimmieson NL. Neck movement and muscle activity characteristics in female office workers with neck pain. Spine 2008;33:555-63. 4. Falla D, Rainoldi A, Merletti R, Jull G. Myoelectric manifestations of sternocleidomastoid and anterior scalene muscle fatigue in chronic neck pain patients. Clin Neurophysiol 2003;114:488-95. 5. Treleaven J. Sensorimotor disturbances in neck disorders affecting postural stability, head and eye movement control. Man Ther 2008;13:2-11. 6. Peolsson A, Kjellman G. Neck muscle endurance in nonspecific patients with neck pain and in patients after anterior cervical decompression and fusion. J Manipulative Physiol Ther 2007;30:343-50. 7. Ylinen J, Takala EP, Kautiainen H, et al. Association of neck pain, disability and neck pain during maximal effort with neck muscle strength and range of movement in women with chronic non‐specific neck pain. Eur J Pain 2004;8:473-8. 8. Fernández-De-Las-Peñas C, Albert-Sanchis JC, Buil M, Benitez JC, Alburquerque-Sendin F. Cross-sectional area of cervical multifidus muscle in females with chronic bilateral neck pain compared to controls. J Orthop Sports Phys Ther 2008;38:175-80. 9. Rezasoltani A, Ali-Reza A, Khosro KK, Abbass R. Preliminary study of neck muscle size and strength measurements in females with chronic non-specific neck pain and healthy control subjects. Man Ther 2010;15:400-3. 10. Panjabi MM, Cholewicki J, Nibu K, Grauer J, Babat LB, Dvorak J. Critical load of the human cervical spine: an in vitro experimental study. Clin Biomech 1998;13:11-7. 11. Wilke HJ, Wolf S, Claes LE, Arand M, Wiesend A. Stability increase of the lumbar spine with different muscle groups. A biomechanical in vitro study. Spine 1995;20:192-8. 12. Falla D, Jull G, Hodges P, Vicenzino B. An endurancestrength training regime is effective in reducing myoelectric manifestations of cervical flexor muscle fatigue in females with chronic neck pain. Clin Neurophysiol 2006;117:828-37. 13. Viljanen M, Malmivaara A, Uitti J, Rinne M, Palmroos P, Laippala P. Effectiveness of dynamic muscle training, relaxation training, or ordinary activity for chronic neck pain: randomised controlled trial. BMJ 2003;327:475. 14. Ylinen J, Takala E-P, Nykänen M, et al. Active neck muscle training in the treatment of chronic neck pain in women. JAMA 2003;289:2509-16. 15. Ylinen JJ, Häkkinen AH, Takala E-P, et al. Effects of neck muscle training in women with chronic neck pain: one-year follow-up study. J Strength Cond Res 2006;20:6-13. 16. Falla D, Jull G, Russell T, Vicenzino B, Hodges P. Effect of neck exercise on sitting posture in patients with chronic neck pain. Phys Ther 2007;87:408-17. 17. Lee J-P, Wang C-L, Shau Y-W, Wang S-F. Measurement of cervical multifidus contraction pattern with ultrasound imaging. J Electromyogr Kinesiol 2009;19:391-7. 18. Peolsson AL, Peolsson MN, Jull GA. Cervical muscle activity during loaded arm lifts in patients 10 years postsurgery for cervical disc disease. J Manipulative Physiol Ther 2011;36:292-9.
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19. Sheard B, Elliott J, Cagnie B, O'Leary S. Evaluating serratus anterior muscle function in neck pain using muscle functional magnetic resonance imaging. J Manipulative Physiol Ther 2012;35:629-35. 20. Zakharova-Luneva E, Jull G, Johnston V, O'Leary S. Altered trapezius muscle behavior in individuals with neck pain and clinical signs of scapular dysfunction. J Manipulative Physiol Ther 2012;35:346-53. 21. Peolsson A, Brodin L-Å, Peolsson M. A tissue velocity ultrasound imaging investigation of the dorsal neck muscles during resisted isometric extension. Man Ther 2010;15:567-73. 22. Kristjansson E. Reliability of ultrasonography for the cervical multifidus muscle in asymptomatic and symptomatic subjects. Man Ther 2004;9:83-8. 23. Lee J-P, Tseng W-YI, Shau Y-W, Wang C-L, Wang H-K, Wang S-F. Measurement of segmental cervical multifidus contraction by ultrasonography in asymptomatic adults. Man Ther 2007;12:286-94. 24. Anderson JS, Hsu AW, Vasavada AN. Morphology, architecture, and biomechanics of human cervical multifidus. Spine 2005;30:E86-91. 25. Danneels L, Vanderstraeten G, Cambier D, et al. Effects of three different training modalities on the cross sectional area of the lumbar multifidus muscle in patients with chronic low back pain. Br J Sports Med 2001;35:186-91. 26. 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;88:1441-5. 27. Muñoz-Muñoz S, Muñoz-García MT, Alburquerque-Sendín F, Arroyo-Morales M, Fernández-de-las-Peñas C. Myofascial trigger points, pain, disability, and sleep quality in individuals with mechanical neck pain. J Manipulative Physiol Ther 2012;35:608-13. 28. Cagnie B, O'leary S, Elliott J, Peeters I, Parlevliet T, Danneels L. Pain-induced changes in the activity of the cervical extensor muscles evaluated by muscle functional magnetic resonance imaging. Clin J Pain 2011;27:392-7. 29. Takasaki H, Hall T, Kaneko S, Iizawa T, Ikemoto Y. Cervical segmental motion induced by shoulder abduction assessed by magnetic resonance imaging. Spine 2009;34:E122-6. 30. Rankin G, Stokes M, Newham D. Size and shape of the posterior neck muscles measured by ultrasound imaging: normal values in males and females of different ages. Man Ther 2005;10:108-15. 31. Moseley GL, Hodges PW, Gandevia SC. Deep and superficial fibers of the lumbar multifidus muscle are differentially active during voluntary arm movements. Spine 2002;27:E29-36. 32. Rezasoltani A, Ahmadipoor A, Khademi-Kalantari K, Javanshir K. The sign of unilateral neck semispinalis capitis muscle atrophy in patients with chronic non-specific neck pain. J Back Musculoskelet Rehabil 2012;25:67-72. 33. Peolsson A, Löfstedt T, Trygg J, Peolsson M. Ultrasound imaging with speckle tracking of cervical muscle deformation and deformation rate: isometric contraction of patients after anterior cervical decompression and fusion for cervical disc disease and controls. Man Ther 2012;17:519-25. 34. Osborn W, Jull G. Patients with non-specific neck disorders commonly report upper limb disability. Man Ther 2013;18:492-7. 35. McLean SM, Moffett JK, Sharp DM, Gardiner E. An investigation to determine the association between neck pain and upper limb disability for patients with non-specific neck pain: a secondary analysis. Man Ther 2011;16:434-9. 36. Lin Y-C, Lai C-H, Chang W-H, Tu L-W, Lin J-C, Chou S-W. Immediate effects of ischemic compression on neck function in patients with cervicogenic cephalic syndrome. J Manipulative Physiol Ther 2012;35:301-7.
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Farhang NooriKochi, MD, d and Alireza Akbarzadeh Baghban, PhD e
ABSTRACT Objective: The purposes of this study were to (1) measure the thickness of cervical multifidus muscle (CMM) in different maximal voluntary contraction percentages of isometric contraction of shoulder muscles, (2) evaluate the differences of the CMM thickness in different directions of the shoulder movement, and (3) compare the changes in the CMM thickness of participants with neck pain and also of healthy individuals. Methods: Twenty healthy men (age, 27.45 ± 4.37 years; height, 177 ± 4.66 cm; weight, 72.85 ± 6.46 kg) and 20 men with chronic mechanical neck pain (age, 28.90 ± 5.53 years; height, 176 ± 5.98 cm; weight, 73.15 ± 7.82 kg) participated in the study. Both the right and left CMM thicknesses were measured using an ultrasound device while participants performed isometric contraction of shoulder muscles in 6 movement directions. Results: In both groups, an increment of CMM thickness followed as the increase of isometric force (P b .01).The increase of muscle thickness of healthy participants was substantially more than the chronic mechanical neck pain participants (P = .03). Although no significant difference of CMM thickness was seen among the effects of the 6 force directions (P N .05), there was a significant difference of activity noted between the left and right sides (P = .047). Conclusion: The results of the present study indicate that isometric contraction of shoulder muscles caused an increase in the CMM thickness regardless of force direction. This increase was seen in both groups of healthy participants and patients with neck pain. However, less thickness changes were observed in participants with neck pain, which may be interpreted as reduced CMM activity in such people. (J Manipulative Physiol Ther 2015;38:210-217) Key Indexing Terms: Ultrasonography; Neck Muscle; Neck Pain; Isometric Contraction; Muscle Size; Shoulder
articipants with chronic neck pain have altered neck muscle activities compared with healthy participants. 1–4 Proprioceptive deficit, sensorimotor disturbances, 5 reduced neck muscle strength, and endurance 6,7 are general
P a
Assistant Professor of Physiotherapy, Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran. b Professor of Physiotherapy, Faculty of Rehabilitation, Physiotherapy Research Center, Shahid Behesht University of Medical Sciences, Tehran, Iran. c Assistant Professor of Physiotherapy, Faculty of Rehabilitation, Department of Physiotherapy, Shahid Behesht University of Medical Sciences, Tehran, Iran. d Radiologist, Specialist Doctor, Department of Radiology, Medical Imaging Research Center, Shiraz University of Medical sciences, Shiraz, Iran.
manifestations of chronic neck pain. Recently, atrophic changes and reduced deep cervical muscles size and thickness have been reported in these participants. 8,9 Because deep dorsal neck muscles including the cervical multifidus muscle e
Associate Professor of Biostatistics, Faculty of Rehabilitation, Department of Basic Sciences, Shahid Behesht University of Medical Sciences, Tehran, Iran. Submit requests for reprints to: Leila Rahnama, PT, PhD, Assistant Professor of Physiotherapy, Deprtment of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran. (e-mail: [email protected] [email protected]). Paper submitted May 16, 2013; in revised form November 6, 2014; accepted November 10, 2014. 0161-4754 Copyright © 2015 by National University of Health Sciences. http://dx.doi.org/10.1016/j.jmpt.2014.11.008
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(CMM) have been shown to play a role in providing neck stability and preventing strains to cervical structures, 10,11 strengthening them is of prime concern while treating patients. Several studies have shown that physical exercises might facilitate increase in muscle strength and improve muscle activity. 4,12–15 However, these studies focused on general training of neck muscles rather than exercises for a selected muscle like CMM. 15,16 Therefore, there is still a need to further expand knowledge concerning activities for each neck muscle. Some studies have targeted areas of the neck. Lee et al 17 reported changes in CMM thickness as an effect of isometric head extension at different levels of the cervical spine in healthy participants. Peolsson et al 18 measured the different activity patterns of cervical muscles, especially for the CMM, during a loaded arm lifting task between healthy participants and patients with long-standing neck pain. What these studies did not investigate, however, is the behavior of the CMM contraction and how it responds to different amounts of force exerted by the shoulder muscles and also the different movement directions of the upper extremities. Various methods are used to investigate neck muscles functions, such as magnetic resonance imaging and ultrasound imaging. 18–20 Among these, ultrasound imaging is recognized as a reliable and valid method of muscle function evaluation in real time. 9,21–23 In recent research studies, the interest in ultrasonography measurement of muscle dimensions has greatly increased. For instance, some studies reported dimensions of the CMM at rest or during an isometric head extension as an index for muscle activity using ultrasound. 8,17,24 However, it is unknown whether the CMM dimensions change during a task involving the upper extremities of patients with chronic neck pain. Further studies are required to reveal this little known aspect of neck muscles functions. We hypothesized that the CMM thickness will change during an isometric contraction of the shoulder muscles in different movement directions in healthy participants more than that of participants with neck pain. Therefore, the purposes of this study were to (1) measure the thickness of CMM in different maximal voluntary contraction (MVC) percentages of isometric contraction of shoulder muscles, (2) evaluate the differences of the CMM thickness in different directions of the shoulder movement, and (3) compare the changes in the CMM thickness of participants with neck pain and also of healthy individuals.
METHODS Participants Twenty participants with chronic mechanical neck pain (CMNP) and 20 healthy individuals voluntarily participated in the study. Participants were recruited from bank office workers. A total of 300 questionnaires containing the study
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Fig 1. Inclusion and exclusion criteria for participants of the study. criteria were distributed among them. Then, the researcher collected the questionnaires and announced those who met the eligibility criteria and stated that they agree to participate in the study. Participants were all male and at least 18 years old with no regular gym activity. The general eligibility criteria include having no any history of trauma or surgery on the spine, any congenital or inflammatory diseases, or shoulder and arm pain. The inclusion and exclusion criteria for participants are listed in Figure 1. Participants in both groups were comparable in terms of age, weight, height, and body mass index (BMI). The procedure was explained to the participants, and they signed the informed consent forms prior to the study. This study was approved by the Research Ethics Board of the Faculty of Rehabilitation, Shahid Beheshti University of Medical Sciences.
Ultrasonography Measurements Ultrasonographic imaging of the CMM was conducted by an ultrasonography device (Accuvix V20 prestige; Samsung, Medison, Korea) with a 8-MHz, 4 .5-cm linear array transducer. An experienced physical therapist identified the spinous process of C4 by palpation. Further clarification was carried out with the help of ultrasonography. We evaluated the CMM at the level of C4, as it has been reported to have a greater cross-sectional area (CSA) than C3 and the same CSA as C5 and C6. 8 Lee et al 23 also investigated the thickness of CMM at the level of C4. At that point, the examiner placed the transducer transversely at the level of the C4 spinous process, moving it slowly to the right or left side and slightly upward and downward so as to identify the echogenic vertebral lamina clearly. At this level, the CMM was located laterally to the spinous process, rotator muscle, and laminar junction;
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Fig 2. Ultrasonographic image of CMM at level C4. medially to the articular process; and just below the fascia of the semispinalis cervicis muscle. 17 The distance from the echogenic vertebral lamina to the interfacing fascia of semispinalis cervicis muscle was measured from border to border at the widest distance as the anterior-posterior dimension (APD) or the thickness of the CMM. The images were taken firstly while the participants were at rest and then with applied force to reach their MVCs of the right shoulder muscles in 6 movement directions (Fig 2).
Muscle Strength The shoulder muscles strength was recorded by a load cell model H3-C3-100 Kg-3B (ZEMIC, Shaanxi, China). The load cell was positioned on a U-shaped groove installed on an arm rest and fixed onto the right side of a custom-made chair so the participants could put their right forearms on it. The groove was designed in a way that allowed the load cell to move in order to record the forces in 6 directions of shoulder movements (flexion, extension, external rotation, internal rotation, abduction, and adduction). The participants were then asked to perform isometric contraction of the shoulder muscles in 6 desired directions and gradually reach their MVCs.
Experimental Procedure Participants were seated relaxed on a chair while keeping their heads and necks in a neutral position and their dominant (right) forearms laid on the armrest. Two thorax and pelvic belts were used to secure participants in the chair (Fig 3). The belts were fastened at the level of the scapular spine and iliac crest, respectively. Then the procedure was completely explained to the participants, and they were asked to perform 3 trial runs of randomly chosen directions to make sure that they were acquainted with the procedure. To start the experimental procedure, the participants were asked to push their right forearms onto the loadcell and
Fig 3. The position of participants during the experimental procedure. (Color version of figure is available online.)
increase their force gradually to reach their MVCs in 10 seconds. Three trials in each force direction were performed with 1-minute intervals between each trial. Then after a 2-minute interval, the next force direction was applied. After completing the procedure in all 6 directions, the participants were given a 15-minute rest before repeating the actions conducive to the evaluation of the effects of isometric contraction of the right shoulder muscles on the left CMM. The trials with maximum force in each direction were selected for data analysis. Then the amount of identical force for 25%, 50%, 75%, and 100% of MVC were identified by a custom-made software for later analysis.
Sonosynch Software A custom-designed software with a sampling rate of 20 per second was used to pick up and store the load cell data and ultrasound images in a synchronized way to enable the examiner to analyze the data offline. The software could pick out and store 20 force data and 20 identical ultrasound images in a second. Therefore, the examiner was provided with forces which ranged from 0 to 100% MVCs and their identical images for data analysis. The distance from the echogenic vertebral lamina to the interfacing fascia of semispinalis cervicis muscle was measured border to border at the widest distance, as was the anterior-posterior dimension or the thickness of CMM.
Reliability Study For the examiner to assess the repeatability of the right CMM thickness measurement at rest and 100% MVC
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Table 1. Comparison of MVC of Shoulder Muscles in Newton (N; Mean ± SD) in 6 Movement Directions of the Shoulder Joint Between the 2 Groups Abduction Adduction Flexion Extension External rotation Internal rotation
Healthy
Participants With CMNP
P
14.91 ± 3.67 14.57 ± 5.71 14.37 ± 6.44 10.93 ± 3.48 10.54 ± 2.30 14.25 ± 4.85
14.01 ± 4.11 14.03 ± 5.28 12.08 ± 4.25 10.30 ± 2.52 10.68 ± 3.51 12.86 ± 4.22
.48 .76 .19 .52 .88 .34
CMNP, chronic mechanical neck pain.
and the maximum strength of the shoulder muscles, the intratester reliability was carried out on both groups, obtaining the data collected on 2 separate occasions of which were collected 3 to 7 days apart. A total number of 24 participants were included (12 healthy and 12 participant with neck pain).
Statistical Analysis The statistical analysis was performed with SPSS software (version 16; SPSS Inc, Chicago, IL). An Independent t test was used to compare the participants' anthropometric data and the isometric force of shoulder muscles between the 2 groups. To assess the reliability of the muscle thickness measurement and the shoulder muscle force, intraclass correlation coefficient (ICC) was used to determine relative reliability and the SEM, and the smallest detectable difference (SDD) were used to determine absolute reliability. The Bland and Altman plot was used to determine the measurements agreement on 2 occasions. The mean differences of measurements on 2 occasions were organized as a reference line on a y axis and ± 1.96 times the SD as limits of agreement. A multifactorial analysis of variance for repeated measures with force (0, 25%, 50%, 75%, and 100% MVC), direction (6 movement directions of the shoulder joint), and side (the right and left CMM) as 3 within factors and group (participants with CMNP and healthy controls) as the between factor was used to evaluate changes in the CMM thickness. The assumption of sphericity has not been met. An α of .05 was taken as the level of significance.
RESULTS Twenty participants with CMNP (age, 28.90 ± 5.53 years; height, 176 ± 5.98 cm; weight, 73.15 ± 7.82 kg; BMI, 23.44 ± 1.59 kg/m 2) and 20 healthy individuals (age, 27.45 ± 4.37 years; height, 177 ± 4.66 cm; weight, 72.85 ± 6.46 kg; BMI, 23.28 ± 1.67 kg/m 2) participated in the present study. The independent t test showed no significant difference in age (P = .36), height (P = .81), weight (P = .81), and BMI (P = .75) between the 2 groups.
Fig 4. a, Bland-Altman plot for cervical multifidus thickness at rest measured in 2 separated days for healthy participants. b, Bland-Altman plot for cervical multifidus thickness at rest measured in 2 separated days for participants with CMNP. The independent t test revealed no significant difference for maximum isometric strength of shoulder muscles in none of the 6 directions between the 2 groups (Table 1). The intratester reliability of the right CMM thickness measurement at rest was high in both groups, with ICC of 0.89 and 0.84, SEM of 0.05 and 0.04, and SDD of 0.14 and 0.11 in healthy participants and participants with CMNP, respectively. As for the reliability of the right CMM thickness measurement at 100% MVC in 6 movement directions in both groups, the reliability was also high, with an ICC ranging from 0.75 to 0.90, SEM ranging from 0.04 to 0.06, and SDD ranging from 0.11 to 0.17. Similarly, the reliability of the maximum muscles strength at 100% MVC of shoulder muscles in all directions was high, with ICC ranging from 0.75 to 0.99, SEM ranging from 0.63 to 2.10, and SDD ranging from 1.74 to 5.82. The agreement between the measurements for CMM thickness at rest on 2 occasions is demonstrated in Figure 4a for healthy participants and in Figure 4b for participants with
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Table 2. Mean and SD for Anterior-Posterior Dimension of CMM in Healthy Participants and Participants With Neck Pain Direction Side
MVC %
Healthy participants Right 0 25 50 75 100 Left 0 25 50 75 100 Participants with neck pain Right 0 25 50 75 100 Left 0 25 50 75 100
Abduction
Adduction
Extension
Flexion
External Rotation
Internal Rotation
1.09 ± 0.17 1.15 ± 0.15 1.15 ± 0.15 1.15 ± 0.15 1.17 ± 0.21 1.07 ± 0.15 1.12 ± 0.15 1.12 ± 0.15 1.12 ± 0.15 1.14 ± 0.15
1.09 ± 0.17 1.10 ± 0.16 1.11 ± 0.16 1.12 ± 0.17 1.13 ± 0.17 1.07 ± 0.15 1.09 ± 0.16 1.10 ± 0.16 1.10 ± 0.18 1.11 ± 0.15
1.09 ± 0.17 1.12 ± 0.17 1.10 ± 0.17 1.14 ± 0.15 1.15 ± 0.16 1.07 ± 0.15 1.12 ± 0.15 1.12 ± 0.15 1.12 ± 0.16 1.14 ± 0.18
1.09 ± 0.17 1.11 ± 0.17 1.13 ± 0.17 1.13 ± 0.17 1.15 ± 0.14 1.07 ± 0.15 1.09 ± 0.12 1.10 ± 0.14 1.08 ± 0.12 1.11 ± 0.12
1.09 ± 0.17 1.13 ± 0.15 1.15 ± 0.14 1.16 ± 0.14 1.17 ± 0.14 1.07 ± 0.15 1.08 ± 0.18 1.08 ± 0.18 1.08 ± 0.19 1.11 ± 0.18
1.09 ± 0.17 1.11 ± 0.15 1.13 ± 0.17 1.13 ± 0.18 1.13 ± 0.16 1.07 ± 0.15 1.11 ± 0.14 1.09 ± 0.15 1.08 ± 0.16 1.12 ± 0.18
1.13 ± 0.16 1.16 ± 0.16 1.15 ± 0.18 1.18 ± 0.15 1.16 ± 0.16 1.09 ± 0.17 1.09 ± 0.13 1.10 ± 0.14 1.08 ± 0.14 1.11 ± 0.15
1.13 ± 0.16 1.15 ± 0.16 1.15 ± 0.17 1.15 ± 0.16 1.17 ± 0.17 1.09 ± 0.17 1.14 ± 0.16 1.12 ± 0.17 1.10 ± 0.17 1.13 ± 0.14
1.13 ± 0.16 1.13 ± 0.17 1.14 ± 0.16 1.16 ± 0.16 1.17 ± 0.16 1.09 ± 0.17 1.09 ± 0.11 1.10 ± 0.12 1.11 ± 0.15 1.11 ± 0.16
1.13 ± 0.16 1.13 ± 0.16 1.14 ± 0.18 1.15 ± 0.16 1.13 ± 0.17 1.09 ± 0.17 1.12 ± 0.15 1.12 ± 0.16 1.11 ± 0.15 1.10 ± 0.14
1.13 ± 0.16 1.12 ± 0.15 1.16 ± 0.16 1.17 ± 0.18 1.15 ± 0.19 1.09 ± 0.17 1.10 ± 0.17 1.08 ± 0.18 1.09 ± 0.18 1.10 ± 0.16
1.13 ± 0.16 1.16 ± 0.15 1.15 ± 0.16 1.15 ± 0.16 1.16 ± 0.14 1.09 ± 0.17 1.12 ± 0.13 1.11 ± 0.14 1.13 ± 0.13 1.13 ± 0.15
%MVC, percent of maximum voluntary contraction.
CMNP. The mean differences were − 0.005 with 95% confidence interval of − 0.195 to 0.185 cm and 0.0005 with 95% confidence interval of − 0.1545 to 0.1555 cm for healthy participants and participants with CMNP, respectively, indicating an acceptable to good levels of agreement between the 2 measurements. The CMM thickness was not significantly different at the baseline between the 2 groups. The mean and SD of the CMM thickness in both groups are presented in Table 2. The mean and SD of the visual analog scale and the neck disability index (NDI) were 4.9 ± 1.8 and 13.4% ± 5.95%, respectively, in the group of chronic pain participants. The results of our study have shown that there was a significant main effect of force on the CMM thickness (F1.47,55.78 = 13.72, P b .001). It demonstrated an increased thickness as the shoulder muscles' strength increased to reach 100% MVC. The main effect of each side was also statistically significant (F1,38 = 4.23, P = .047), indicating that the CMM thickness on the right side underwent more changes compared with the left side. The interaction of group by force was significant (F1.47,55.78 = 2.81, P = .027), indicating a more considerable increase in the CMM thickness during isometric contraction of the shoulder muscles in healthy participants than in participants with CMNP. No other main or interaction effects for CMM thickness were significant for a group (F1,38 = 0.12, P = .73), direction (F3.81,144.97 = 0.43, P = .83), group by direction (F3.81, 144.97 = 1.30, P = .26), direction by force (F10.34, 392.87 = 0.67, P = .86), side by direction (F5,190 = 1.42, P = .22), side by force (F1.50,57.14 = 0.71, P = .59), group by force by direction
(F10.34,392.87, P = .15), group by direction by side (F4.31,163.78, P = .76), side by direction by force (F10.53,400.23 = 1.02, P = .43), force by side by group (F1.50,57.14 = 0.08, P = .99), and force by group by direction by side (F10.53,400.23 = 0.72, P = .81).
DISCUSSION We found out that CMM thickness increased while isometric force of the shoulder muscles increased. This finding is seen in both groups. A possible underlying mechanism for this finding is that the CMM is a cervical stabilizer, 24 so it is possibly contracted during performance of tasks by the upper extremities to stabilize the cervical spine. Such findings have been previously reported for the lumbar multifidus muscle. Danneels et al 25 reported an increase in the CSA of the lumbar multifidus muscle after a period of resistive training of the lower extremities. This finding is consistent with previous reports that the deep neck extensor muscles including CMM are activated during a lifting task to support the cervical spine. 18 A novel aspect of this study was evaluating differences of the thickness of CMM during isometric contraction of the shoulder muscles between participants with CMNP and healthy controls. According to our results, the interaction of force by group was significant for the CMM thickness. It implies that isometric contraction of shoulder muscles led to different changes in the CMM thickness in participants with neck pain and healthy participants regardless of the force direction and the side of CMM. We found that an increase
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in force production by the shoulder muscles led to an increase in the CMM thickness, although in healthy participants, the muscle thickness increased more considerably than that in participants with neck pain. This observed difference between the 2 groups may be because participants with neck pain confront a lot of physiological changes such as a weakness of deep muscles, 1,9,26 prompting their inability to activate their CMM as much as healthy individuals. A further problem associated with CMNP is the presence of active trigger points in the deep extensor muscles of participants with CMNP, which may cause restriction of the deep extensor muscles activation in such a population. 27 Our results also support those of Cagnie et al, 28 who showed a reduced activity of the CMM during a cervical extension task in an experimentally pain-induced condition when compared with a no-pain condition. However, our results are not in line with the results of the study conducted by Peolsson et al, 18 who found a greater deformation rate of the CMM during a loaded arm lifting task in participants with long-standing pain than in healthy individuals. Because it was demonstrated that there is a linear correlation between the degree of muscle contraction and the corresponding degree of muscle deformation, we can conclude that the greater muscle deformation rate in participants underwent anterior cervical decompression and fusion in the study by Peolsson et al indicates a higher muscle contraction in such participants. Our findings do not support this either. A different population undergoing the study or a different evaluation method of the muscle function might explain the discrepancy of the results. Findings by Peolsson et al 18 are notable due to illustration of an altered behavior in deep neck muscles of participants with long-standing neck pain. This implies altered motor strategies to support the cervical spine in such participants. Alternatively, Sheard et al 19 found altered activity and length-tension relations of the trapezius and the levator scapula in patients with neck pain. 20 These muscles have expanded attachments to the cervical spine, making the cervical vertebrae rotate during tasks performed by the upper extremities. 29 As a result, their altered length-tension relations may affect the amount and the nature of the vertebral motions. This may lead to an altered function of deep neck muscles like the CMM, aiming to stabilize the cervical spine in participants with neck pain. This study demonstrated that the mean thickness of the CMM on the right side was statistically larger than that of the left side at the level of C4. This might be because all participants in the present study were right handed. This finding is not in agreement with that of Fernández-de-las-Peñas et al, 8 who reported no statistically significant difference between the CSA of CMM on the 2 sides. However, their reported CSA of CMM on the right side was greater than the left one. Rankin et al 30 have also reported the symmetry of CMM between the 2 sides. The disagreement between the results could be because we measured the thickness of CMM while researchers of previous studies measured the CSA of CMM, which had been affected by muscle thickness and other dimensions of the muscle.
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The main effect of direction was not significant, concluding that the isometric contraction of shoulder muscles in all 6 directions had the same effect on the CMM thickness. These results are expectable because it has been claimed that the multifidus muscle provides the stability of the spine regardless of the direction of movement. 31 No statistically significant baseline difference in the thickness of CMM was seen in participants with CMNP when compared with healthy people. This result does not support the findings of Kristjansson, 22 who showed a reduced thickness of CMM in participants with neck pain. This discrepancy of the result may be due to the different group of participants involved in the study. Kristjansson evaluated people with chronic whiplash-associated disorder, whereas our participants had experienced neck pain for 3 months in the last year. Some have argued that neck pain may cause muscle atrophy via reflex. 32 Although this short period of pain experienced by our tested participants may not be long enough to change the muscle, patients participating in the study by Kristjansson et al had a higher disability index than did our participants and a higher age range. This is justifiable because the greater the duration of neck pain, the greater NDI and probably more atrophy in muscles. 8 Fernández-de-las-Peñas et al also found a smaller CSA in patients with neck pain compared with healthy people. This is not in agreement with our study, as participants in their study had a mean NDI of 27.6, whereas our participants had the mean NDI of 13.6, almost half the patients studied by Fernández-de-las-Peñas et al. 8 The isometric forces of shoulder muscles in 6 movement directions in participants with neck pain were not significantly different with healthy individuals. This result was expectable as participants with CMNP had no pain or discomfort in their shoulder area. Therefore, the isometric strength of their shoulder muscles was equal to their healthy controls. Similarly, Peolsson et al 33 found no significant difference in neck muscle strength during an isometric contraction of neck muscles between healthy participants and participants with long-standing neck pain. However, they argued at the small size of the examined population and on the large interindividual differences as possible cause of such similarities. Both arguments are not applicable to our case study. Our results do not support the findings presented by Osborn and Jull 34 where it shows that neck pain is in association with upper limb disability. They reported a moderate to high relationship between the NDI and upper limb disability. Our results are reasonable as the participants in their study had a mean NDI of 27.7, whereas our participants had the mean NDI of 13.4, which is almost half the NDI of those participants. We saw no difference in the shoulder muscle strengths between the 2 groups. Some activities reported as to be difficult or to be disturbing to participants in aforementioned study were those needing the neck to be extended or flexed, such as overhead activities and gardening, whereas participants in our study kept their neck in a neutral position during the
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experimental procedure. This enabled them to do the isometric task of shoulder muscles with no induced pain or restriction. Osborn and Jull presented that patients with neck and arm pain demonstrated more upper limb disability than participants with neck pain only. It is notable that our participant population had no arm or shoulder pain. Our findings do not support the results of the study by McLean et al 35 demonstrating upper limb disability in patients with neck pain. The mostly high level of disability (mean Northwick Park Neck Pain Questionnaire of 38.7) in patients participating in their study may explain the reason for the different findings. We also evaluated the intraexaminer reliability in measuring the CMM thickness to assess the accuracy of the results. Our results also showed that the intraexaminer reliability of measuring the CMM thickness was high both at rest and during contraction in healthy participants and patients with neck pain. Similar reports of the reliability for CMM ultrasonography have already been reported. 22 Lee et al 23 also reported ultrasonography measurement of the thickness of CMM by an examiner as a reliable and valid method to evaluate CMM function.
LIMITATIONS Male participants were only considered in the present study. It is recommended to compare current results with deep neck muscles behavior in women. Another limitation is that the isometric task did not resemble functional tasks and did not represent normal function of neck muscles. Future studies may be needed to compare the activity of CMM in response to daily tasks in both men and women. The results of this study cannot be generalized to all participants with neck pain, as we only evaluated participants with CMNP and an average visual analog scale score of 4.9. To permit a more generalized interpretation, a population-based epidemiologic study is needed. The case-control design of the study did not allow us to evaluate the training effect of isometric contraction of shoulder muscles on CMM thickness; future clinical trials should address this issue. Further studies may also be required to determine the effect of hand dominancy on the size of CMM. Finally, the sitting position of our participants in the present study was a comfortable condition, letting them focus on their shoulders isometric forces. Evaluating the CMM responses to a task of the upper extremities during a more challenging position like standing may shed more light on the stabilizer role of the CMM, when it has to send more afferent information to the brain affecting postural stability. 36
CONCLUSION The results of the present study suggest that isometric contraction of shoulder muscles causes an increase in the CMM thickness regardless of force direction. This increase was seen in both groups of healthy participants and patients with neck pain. However, less thickness changes were
Journal of Manipulative and Physiological Therapeutics March/April 2015
observed in participants with neck pain, which may be interpreted as reduced CMM activity in such people.
Practical Applications • The CMM thickness increased during the isometric contraction of shoulder muscles in all 6 directions of shoulder movements. • The changes in CMM thickness were seen both in healthy participants and people with chronic neck pain. • The CMM thickness increased while the isometric contraction of shoulder muscles increased to reach 100% MVC. • Patients with chronic neck pain showed lesser changes in CMM thickness compared with healthy individuals.
ACKNOWLEDGMENT We thank the manager of Marvdasht Physiotherapy Clinic, Ms Manizheh Saberi, PT, for her assistance in enrolling and screening the participants of the study.
FUNDING SOURCES AND POTENTIAL CONFLICTS OF INTEREST No funding sources or conflicts of interest were reported for this study.
CONTRIBUTORSHIP INFORMATION Concept development (provided idea for the research): A.R., and L.R. Design (planned the methods to generate the results): L.R., and A.R. Supervision (provided oversight, responsible for organization and implementation, writing of the manuscript): A.R., and M.K.h. Data collection/processing (responsible for experiments, patient management, organization, or reporting data): L.R., and F.N. Analysis/interpretation (responsible for statistical analysis, evaluation, and presentation of the results): L.R., and A.A. Literature search (performed the literature search): L.R. Writing (responsible for writing a substantive part of the manuscript): L.R. Critical review (revised manuscript for intellectual content, this does not relate to spelling and grammar checking): L.R., A.R., M.K.h., and F.N.
Journal of Manipulative and Physiological Therapeutics Volume 38, Number 3
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