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Journal of Back and Musculoskeletal Rehabilitation 28 (2015) 833–840 DOI 10.3233/BMR-150593 IOS Press
The effect of different exercise programs on cervical flexor muscles dimensions in patients with chronic neck pain Khodabakhsh Javanshira, Mohsen Amirib , Mohammad Ali Mohseni Bandpeic,f,∗, Cesar Fernandez De las Penasd and Asghar Rezasoltanie a
Department of Physiotherapy, Babol University of Medical Sciences, Babol, Iran Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Evin, Tehran, Iran c Iranian Research Center on Aging, Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Evin, Tehran, Iran d Department of Physical Therapy, Occupational Therapy, Rehabilitation and Physical Medicine, Universidad Rey Juan Carlos, Alcorcon, Madrid, Spain e Department of Physiotherapy, Faculty of Rehabilitation, Shahid Beheshti University of Medical Sciences, Tehran, Iran f University Institute of Physical Therapy, Faculty of Allied Health Sciences, University of Lahore, Lahore, Pakistan b
Abstract. OBJECTIVE: The effect of different exercise programs on cervical flexor muscles dimensions in patients with chronic neck pain is yet to be demonstrated. The purpose of this study was to assess the effect of two exercise programs; craniocervical flexion (CCF) and cervical flexion (CF), on flexor muscles dimensions in patients with chronic neck pain. METHODS: Following ethical approval, 60 patients were randomly assigned into either a CCF group or a CF group. Patients in the CCF group were given CCF exercises and those in the CF group received CF exercises. All patients received interventions for a period of ten weeks. Pain intensity and functional disability were assessed using numerical pain rate scale and neck disability index, respectively. Dimensions of longus colli (LC) and sternoclidomastoid (SCM) muscles were measured using ultrasonography (US). All measurements were taken before and after interventions. RESULTS: Following intervention, the CCF group demonstrated a significant increase in LC muscle dimensions including cross sectional area, width and thickness compared with the CF group. A statistically significant increase was found on SCM thickness in the CF group. Following intervention, SCM thickness measurement in the CCF group showed no significant changes. Statistically significant decrease on pain intensity and disability were also found in both groups. CONCLUSION: Present findings demonstrated that craniocervical flexion program which specifically recruiting deep cervical flexor muscles increased LC muscle dimension significantly and CF program as an endurance training program increased SCM thickness. Keywords: Exercise program, ultrasonography, neck pain, flexor muscles, cross sectional area
1. Introduction
∗ Corresponding author: Mohammad A. Mohseni-Bandpei, Iranian Research Center on Aging, Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, PO Box 1985713834, Evin, Tehran, Iran. E-mail: Mohseni_bandpei@ yahoo.com.
Mechanical neck pain is a prevalent musculoskeletal condition which has a remarkable socioeconomic impact [1,2]. In a study conducted in Canada, about 10% of individuals reported high levels of neck pain and approximately 5% suffered severe disability resulting from neck pain [3]. As regards with the management
c 2015 – IOS Press and the authors. All rights reserved ISSN 1053-8127/15/$35.00
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of neck pain, a considerable number of studies have focused on neck muscles as important elements for stability and mobility of the cervical spine [4,5]. There is a clear role for neck flexors in movement, posture and stabilization of the cervical spine [6]. In fact, stabilization of cervical spine is provided by a muscle sleeve formed by the deep cervical flexors including longus colli (LC) and longus capitis, and the deep posterior neck muscles including semispinalis cervicis, multifidus and rotators. Decreased muscle strength and endurance [6], as well as atrophy of the neck muscles were reported in patients with neck pain [7]. Many studies have shown that muscles changes can be reliably visualized in healthy subjects and patients suffering from different musculoskeletal disorders using ultrasound (US) (e.g. [8–10]). In studies conducted on cervical muscles, some reported muscle atrophy [7,10] and some other demonstrated decreased muscle strength and endurance in patients with neck pain [6]. Studies utilizing electromyography (EMG) have shown delayed activation of deep and superficial neck muscles in patients with neck pain which may be due to altered motor control of the cervical muscles and impaired neck flexor synergy of deep and superficial layers [7]. It is suggested that strengthening exercises may change dimension of neck muscles [4]. Given the relevant role for different layers of flexor muscles in stability and normal biomechanics of the cervical spine, and knowledge of impaired activation and size of these muscles in patients with neck pain, it is likely that different exercise programs may lead to an improvement in muscle size and motor control in patients with chronic neck pain. There are two types of exercise programs for retraining the neck flexors: the low load cranio-cervical flexion (CCF) training regimen and conventional cervical flexor (CF) endurance-strength training program [11]. The former emphasizes on co-ordination between the two layers of neck flexors, having an effect on motor control, and the latter focuses on increasing the endurance and strength of the layers through a high load exercise regimen. As there is a role for deep and superficial cervical flexor muscles in normal biomechanics of the cervical spine, and no published study was found to assess the effect of different exercise programs on neck muscles size, the current study was designed to compare the effects of the two exercise programs on deep and superficial cervical flexor muscles dimensions using US. It was hypothesized that CCF exercise program which
initially concentrates on activation of deep flexors and then on superficial, would exhibit more increase in dimension of deep cervical flexor muscles compared to CF exercise.
2. Methods This study was a single blinded randomized controlled clinical trial in which the assessor was blind throughout the study. 2.1. Subjects The study was approved by the Medical Ethics Board at the University of Social Welfare and Rehabilitation Sciences. Written informed consent was obtained from all participants. Sixty (n = 60) subjects (20 male, 40 female, mean ± SD age: 38 ± 4 years) have participated. Subjects were recruited from patients referring to the physiotherapy clinic of University of Social Welfare and Rehabilitation Sciences. Participants were included if they had a history of chronic, nonspecific neck pain of more than 3 months as well as a palpable tenderness on cervical joints. Patients were excluded if they had any history of cervical spine surgery, any cervical trauma (e.g., whiplash), any neurological signs, taking medications or any physiotherapy treatment, or had participated in a neck or shoulder exercise programs within last six months. The sample size was based on previous studies detecting differences of 20% in cross sectional area (CSA) or thickness of multifidus muscle between healthy subjects and patients with chronic neck pain [12]. Assuming a standard deviation of 10%, an alpha level of 0.05, and a desired power of 90%, the sample size generated was 30 subjects in each group. Therefore, the study had sufficient power to detect the effect of exercise intervention on cervical muscles dimensions. The participants were randomly assigned into either a CCF group or a CF group through block style randomization sequence. 2.2. Outcome measures 2.2.1. Muscle dimensions An US device (ultrasonix, medical corp., ES500 Canada) with a 12.5 MHz linear array and 38 mm foot print probe was used. For LC muscle size measurement, the subjects were positioned supine, 2 cm
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2.3. Treatment interventions All subjects performed their exercise program under supervision of an experienced physical therapist 3 times per week for 10 weeks. Maximum duration of any exercise session was 30 min. Subjects were advised not to receive any other specific intervention for their pain along with the interventions of the current study. All subjects were asked to perform exercises 3 times per day during the study. It was reminded that the exercises should be performed with no pain.
Fig. 1. Ultrasonography image of sternoclidomastoid (SCM) and longus colli (LC).
below the thyroid cartilage was marked by a marker, and the image was captured at this level (about C6) in the relaxed state of the muscle [13]. Anterior posterior dimension (APD), lateral dimension (LD) and CSA were measured 3 times and the average was reported. APD of the sternocleidomastoid (SCM) muscle was also measured 3 times in the same position of the patient and transducer (Fig. 1). The mean data was used for further analysis. 2.2.2. Pain intensity and functional disability The mean intensity of neck pain was assessed with an 11-point numerical pain rate scale (NPRS, 0: no current pain, 10: maximum pain) [14]. Cleland et al reported that the minimal detectable change (MDC) and the minimal clinically important difference (MCID) were 1.3 and 2.1 points, respectively for patients with neck pain (15). The neck disability index (NDI) which is a widely accepted disability questionnaire was used to assess functional disability. It contains 10 items, 7 related to activities of daily living, 2 related to pain, and 1 item related to concentration. Each item is scored from 0 to 5. The numeric score for each item is summed for a total score varying from 0 to 50, where higher scores reflect greater disability. The NDI has shown to be reliable and valid for patients with neck pain and has shown a MDC of 20% for patients with neck pain [15]. In present study, NDI was measured using validated Iranian version of related questionnaire [16].
2.3.1. CCF intervention The CCF program was performed according to the protocol described by O’Leary et al. [11]. This exercise seems to activate deep anterior muscles of the cervical spine including LC and longus capitis rather than the superficial flexors, such as SCM and anterior scalene [11]. The exercise is a low load training in order to target specifically deep cervical flexors rather than the neck flexors as a whole which may occur in a high load training of neck flexors. An air-filled pressure sensor held under neck monitored the flattening of the cervical lordosis which caused by longus colli contraction (Fig. 2a). By the feedback from the pressure sensor, subjects were trained to gradually reach 5 pressure targets in 2 mmHg increments from a baseline of 20 mmHg to the final level of 30 mmHg. Subjects were asked to gently nod their head as they were saying “yes”. The maximum pressure level that the subjects could hold steadily without involvement of superficial muscles and without quick jerky CCF movement, was monitored and considered as patients’ level of deep muscle performance. An experienced and qualified physical therapist monitored the contraction and prohibited applying contraction of superficial muscles in all stages of the test using observation and palpation. Training was started at the target level achieved by the subject without any contribution of the superficial flexors (SCM, hyoid and anterior scalene). The subjects were asked to perform a slow and controlled CCF. They trained to increase ranges of CCF using feedback from the pressure sensor placed behind their neck. For each pressure target level, the duration of the contraction was 10 seconds followed by 10 seconds rest, and the subject had to perform the contraction 10 times. Then the subject could progress to the next level.
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(a)
(b)
Fig. 2. Two types of exercise program, a: Craniocervical flexion, b: Cervical flexion (Adopted from O’Leary et al. [11]).
2.3.2. CF intervention In a supine and comfortable resting position of the head, patients were asked to lift up their head through full range of motion as much as possible without any discomfort or reproducing of the symptoms. The upper cervical spine was placed in neutral position and the movement had to be performed slowly through the range (Fig. 2b). The exercise program was divided into two separate stages. According to the recommendation of previous studies for untrained subjects, the duration of the first and second stage was set for 2 and 8 weeks, respectively [11]. For every subject, 12 repetition maximum (RM) was identified at the first session, progressed gradually to 15 RM and this level was maintained for the reminder of the stage. In stage 2, patients performed 3 sets of 15 repetitions of the initial 12 RM, 3 times per day. One minute interval between sets was applied. If patients could perform the exercise easily, then weighted sandbags were added to their forehead with 0.5 kg increments. If the patients were unable to perform exercise easily then the load on neck flexors was reduced by allowing the patients to perform the task with the upper body (trunk and neck) inclined up from the horizontal. In this situation the subjects could do the required repetitions of the movements.
groups using independent t-tests for continuous data and 2 tests of independence for categorical data. Separated 2 × 2 mixed model ANOVAs with time (prepost) as a within-subject variable and group (CCF training and CF training) as the between-subject variable was used to examine the effects of interventions on pain, disability and each muscle dimension outcome. The hypothesis of interest was the Group * Time interaction at -level equal to 0.05. To enable comparison of effect sizes, standardized mean differences (SMDs) was calculated by dividing mean score differences between experimental and control groups by the pooled standard deviation. P values lower than 0.05 were considered as statistically significant for all analyses.
3. Results Sixty patients (20 male, 40 female; mean age: 36 ± 4 years; height: 164 ± 6 cm; weight: 66 ± 10 kg) with mechanical neck pain who met the inclusion/exclusion criteria and agreed to participate, were randomly assigned into either a CCF training group (n = 30) or a CF training group (n = 30). All patients have completed the study. No significant differences were found for baseline clinical features and muscle dimensions between the two groups (Table 1).
2.4. Data analysis 3.1. Changes in neck muscles dimensions Statistical analysis was conducted with the SPSS package version 18.0. Mean, standard deviation and/or 95% confidence intervals for each outcome measure are presented. The Kolmogorov-Smirnov test showed a normal distribution of the data (P > 0.05 in all instances). Baseline features were compared between
After 10 weeks of intervention, significant group * time interactions were found in all muscle outcomes: the CCF training group demonstrated a significant increase in LC muscle dimensions including CSA (F = 28.235; P < 0.001), width (F = 9.863; P = 0.003)
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Table 1 Baseline characteristics of patients in the two groups Craniocervical flexion exercise Mean ± SD Range 36.8 ± 3.5 27–40 3.33 ± 3.22 0.33–12 4.97 ± 2.39 1.5–9.8 33.27 ± 11.4 14–56
Age (y) Pain duration (y) Neck pain intensity VAS (0–10 cm) Neck pain disability (0–100%)
Cervical flexion exercise Mean ± SD Range 35.7 ± 5 19–40 3.32 ± 3.22 0.25–12 5.07 ± 2.15 1.7–9.8 33.2 ± 15 4–68
Table 2 Neck exercise and muscle dimensions in patients with chronic neck pain
Pain intensity Functional disability SCM thickness (mm) LCM CSA cm2 APD mm LD mm
Pre exercise Mean (SD) 4.97 ± 2.39 33.27 ± 11.4 9.300 (2.01) 0.786 (0.04) 8.150 (0.28) 13.89 (0.45)
CCF Post exercise Mean (SD) 2.27 ± 1.51 15.20 ± 9.16 9.300 (1.89) 0.953 (0.05) 9.216 (0.56) 14.810 (0.52)
Diff (mean) 2.70 ± 1.63 18.07 ± 10.2 0.000 0.167 ± 0.02 1.06 ± 0.45 0.92 ± 0.17
Pre exercise Mean (SD) 5.07 ± 2.15 33.2 ± 15.1 9.400 (1.86) 0.790 (0.04) 8.146 (0.25) 13.893 (0.48)
CF Post exercise Mean (SD) 2.75 ± 1.41 19.01 ± 10.1 10.133 (1.77) 0.884 (0.05) 8.900 (0.32) 14.436 (0.46)
Diff (mean) 2.32 ± 1.19 14.2 ± 11.2 0.733 0.094 0.754 0.543
Abbreviations: CCF (craniocervical flexion), CF (cervical flexion), Diff (difference), SD (standard deviation). 1
LCCSA1
0.953
0.95
LCCSA2 0.884
0.9
LCAPD2
9.5
9.216 8.9
9
0.85 0.8
LCAPD1
10
0.79
0.786
8.5
0.75
8.15
8.146
8
0.7
7.5
0.65
7
0.6 0.55
6.5
0.5
C CF
CF
Fig. 3. Pre intervention and post intervention cross sectional area of longus colli.
and thickness (F = 37.634; P < 0.001) compared with CF (Figs 3–5; Table 2), whereas the CF group demonstrated a significant increase (F = 26.167; P < 0.001) in SCM thickness as compared to the CCF group (Fig. 6; Table 2). Between-groups effect sizes were large for SCM thickness (SMD: 1.05) and moderate for LC muscle dimensions (0.65 < SMD < 0.50) 3.2. Changes of pain and disability The 2 × 2 ANOVA demonstrated no significant group * time interactions for neck pain intensity (F = 1.508, P = 0.308) and disability (F = 1.986, P = 0.164): neck pain intensity and disability decreased
6
CCF
CF
Fig. 4. Pre intervention and post intervention anterior and posterior dimensions of longus colli.
similarly in both groups (Table 2). Between-groups effect sizes were small for both outcomes (SMD: 0.35).
4. Discussion The results of this study demonstrated that exercise programs targeting deep cervical flexor muscles (CCF program) increased LC muscle dimensions and CF program tended to increased SCM muscle thickness in individuals with mechanical neck pain. In addition, the exercise programs were equally effective on pain and disability.
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16
LCLD1 14.81
15 14
LCLD2 14.436
13.89
13.893
13 12 11 10
C CF
CF
Fig. 5. Pre intervention and post intervention lateral dimensions of longuss colli.
Fig. 6. Change in sternoclidomastoid (SCM) muscle after CF exercise.
Considering the high recurrence rate of neck pain and the stabilizing function of deep cervical flexors [17], specific exercise programs may have a prohibiting effect on recurrence rate of cervical pain. To the best of the authors’ knowledge, the present study is the first of its kind to assess the effect of specific exercise regimes on the muscle size of the deep cervical flexors utilizing US. It was found that CCF exercise program increased LC muscle dimensions including CSA, thickness and width, whereas the CF exercise program increased SCM thickness only in pa-
tients suffering from mechanical neck pain. It seems that in CCF program the main focus is initially on recruitment of deep cervical flexors, whereas in CF program the patient learns to lift head which leads to general activation of neck flexors including deep and superficial muscles. Evidences emphasize on the importance of deep cervical muscle sleeve for stability of cervical spine [18, 19]. Falla et al. reported deep cervical flexor muscles dysfunction in patients with chronic neck pain. In fact, pain itself and fear of pain may tend to different recruitment pattern of anterior or posterior deep and superficial muscle groups [20]. Abnormal recruitment may result in inhibition of deep layer and hyperactivity of superficial layer. Decreased activity of deep flexors in patients with neck pain may result in diminished support and control of the cervical spine joints and compensatory increase of superficial muscles including anterior scalene and SCM [21]. While EMG findings in neck pain have shown impaired co-ordination of deep and superficial cervical flexors [20] and increased latency of muscle action, studies utilizing US and MRI have demonstrated decreased dimension of the muscles [7,22]. Therefore, it seems that both muscle dimension and motor control may be affected in patients with neck pain. Some studies have pointed out the disturbance of deep and superficial muscles co-ordination resulted in hyperactivity of superficial muscles in patients with neck pain (e.g. [23]). Previous study conducted on comparison of LC muscle dimensions between healthy subjects and patients with chronic neck pain showed that CSA and thickness of LC in patients group were smaller than that of healthy controls [22]. It appears that response to exercise program is greater in weak muscles. Long term training of muscles may alter the recruitment pattern via the neuromuscular control units and repetition of a specific task lead to adaptive changes of the spinal muscles. This idea was supported by Conley et al. [24]. In an MRI study, it was reported that the size of SCM and splenius capitis muscles significantly increased after a period of resistive head and neck extension exercise [24]. After 10 weeks of exercise, similar decreases on pain and perceived disability were found in both groups. Different studies have shown significant relationship between increasing muscle strength and decreasing pain intensity in patients with neck pain [17, 22,23,25]. Also light cervical proprioception exercises showed immediate pain reduction following intervention [26].
K. Javanshir et al. / The effect of different exercise programs on CF muscles dimensions
Several studies demonstrated that different exercise regimes may tend to reduced neck pain immediately post intervention compared with a control group (e.g. [27–29]). In addition, other studies have also indicated that exercise programs reduced disability in patients with neck pain. Falla et al. reported similar reduction in disability after the same two different exercise protocol (strength-endurance training and CCF) on 58 females suffering from chronic neck pain [25]. In another study conducted by Ylinen [29], investigating the effect of different exercise programs, similar immediate decreases in disability was found. The results of the present study are in accordance with previous data, confirming that both exercise programs are equally effective for reducing pain and disability in patients with neck pain. According to the results of the present study, it seems that recruitment of neck flexor muscles in normal pattern within the CCF group resulted in strengthening of deep flexor muscles and increasing of muscle dimensions. The changes of LC muscle in present study may be indicative of an altered capacity of this muscle sleeve to better support the cervical spine in patients suffering from chronic neck pain.
5. Conclusion The results demonstrated that the exercise program targeting the deep neck flexors (CCF program) increased LC muscle dimensions including CSA, thickness and width, whereas the exercise generally recruiting neck flexors (CF program) increased SCM thickness in patients suffering from mechanical neck pain. In addition, exercise programs targeting either the deep cervical flexors or generally deep and superficial muscles were equally effective on pain and disability in individuals with neck pain.
Ethical approval The study was given ethical approval from Medical Ethics Board, at the University of Social Welfare and Rehabilitation Sciences, Tehran, Iran References [1]
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Acknowledgment The authors acknowledge all subjects participating in this study.
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Conflict of interest There is no conflict of interest in this study. Meanwhile, the paper was not previously presented or published in any form anywhere.
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Journal of Back and Musculoskeletal Rehabilitation 28 (2015) 833–840 DOI 10.3233/BMR-150593 IOS Press
The effect of different exercise programs on cervical flexor muscles dimensions in patients with chronic neck pain Khodabakhsh Javanshira, Mohsen Amirib , Mohammad Ali Mohseni Bandpeic,f,∗, Cesar Fernandez De las Penasd and Asghar Rezasoltanie a
Department of Physiotherapy, Babol University of Medical Sciences, Babol, Iran Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Evin, Tehran, Iran c Iranian Research Center on Aging, Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Evin, Tehran, Iran d Department of Physical Therapy, Occupational Therapy, Rehabilitation and Physical Medicine, Universidad Rey Juan Carlos, Alcorcon, Madrid, Spain e Department of Physiotherapy, Faculty of Rehabilitation, Shahid Beheshti University of Medical Sciences, Tehran, Iran f University Institute of Physical Therapy, Faculty of Allied Health Sciences, University of Lahore, Lahore, Pakistan b
Abstract. OBJECTIVE: The effect of different exercise programs on cervical flexor muscles dimensions in patients with chronic neck pain is yet to be demonstrated. The purpose of this study was to assess the effect of two exercise programs; craniocervical flexion (CCF) and cervical flexion (CF), on flexor muscles dimensions in patients with chronic neck pain. METHODS: Following ethical approval, 60 patients were randomly assigned into either a CCF group or a CF group. Patients in the CCF group were given CCF exercises and those in the CF group received CF exercises. All patients received interventions for a period of ten weeks. Pain intensity and functional disability were assessed using numerical pain rate scale and neck disability index, respectively. Dimensions of longus colli (LC) and sternoclidomastoid (SCM) muscles were measured using ultrasonography (US). All measurements were taken before and after interventions. RESULTS: Following intervention, the CCF group demonstrated a significant increase in LC muscle dimensions including cross sectional area, width and thickness compared with the CF group. A statistically significant increase was found on SCM thickness in the CF group. Following intervention, SCM thickness measurement in the CCF group showed no significant changes. Statistically significant decrease on pain intensity and disability were also found in both groups. CONCLUSION: Present findings demonstrated that craniocervical flexion program which specifically recruiting deep cervical flexor muscles increased LC muscle dimension significantly and CF program as an endurance training program increased SCM thickness. Keywords: Exercise program, ultrasonography, neck pain, flexor muscles, cross sectional area
1. Introduction
∗ Corresponding author: Mohammad A. Mohseni-Bandpei, Iranian Research Center on Aging, Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, PO Box 1985713834, Evin, Tehran, Iran. E-mail: Mohseni_bandpei@ yahoo.com.
Mechanical neck pain is a prevalent musculoskeletal condition which has a remarkable socioeconomic impact [1,2]. In a study conducted in Canada, about 10% of individuals reported high levels of neck pain and approximately 5% suffered severe disability resulting from neck pain [3]. As regards with the management
c 2015 – IOS Press and the authors. All rights reserved ISSN 1053-8127/15/$35.00
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of neck pain, a considerable number of studies have focused on neck muscles as important elements for stability and mobility of the cervical spine [4,5]. There is a clear role for neck flexors in movement, posture and stabilization of the cervical spine [6]. In fact, stabilization of cervical spine is provided by a muscle sleeve formed by the deep cervical flexors including longus colli (LC) and longus capitis, and the deep posterior neck muscles including semispinalis cervicis, multifidus and rotators. Decreased muscle strength and endurance [6], as well as atrophy of the neck muscles were reported in patients with neck pain [7]. Many studies have shown that muscles changes can be reliably visualized in healthy subjects and patients suffering from different musculoskeletal disorders using ultrasound (US) (e.g. [8–10]). In studies conducted on cervical muscles, some reported muscle atrophy [7,10] and some other demonstrated decreased muscle strength and endurance in patients with neck pain [6]. Studies utilizing electromyography (EMG) have shown delayed activation of deep and superficial neck muscles in patients with neck pain which may be due to altered motor control of the cervical muscles and impaired neck flexor synergy of deep and superficial layers [7]. It is suggested that strengthening exercises may change dimension of neck muscles [4]. Given the relevant role for different layers of flexor muscles in stability and normal biomechanics of the cervical spine, and knowledge of impaired activation and size of these muscles in patients with neck pain, it is likely that different exercise programs may lead to an improvement in muscle size and motor control in patients with chronic neck pain. There are two types of exercise programs for retraining the neck flexors: the low load cranio-cervical flexion (CCF) training regimen and conventional cervical flexor (CF) endurance-strength training program [11]. The former emphasizes on co-ordination between the two layers of neck flexors, having an effect on motor control, and the latter focuses on increasing the endurance and strength of the layers through a high load exercise regimen. As there is a role for deep and superficial cervical flexor muscles in normal biomechanics of the cervical spine, and no published study was found to assess the effect of different exercise programs on neck muscles size, the current study was designed to compare the effects of the two exercise programs on deep and superficial cervical flexor muscles dimensions using US. It was hypothesized that CCF exercise program which
initially concentrates on activation of deep flexors and then on superficial, would exhibit more increase in dimension of deep cervical flexor muscles compared to CF exercise.
2. Methods This study was a single blinded randomized controlled clinical trial in which the assessor was blind throughout the study. 2.1. Subjects The study was approved by the Medical Ethics Board at the University of Social Welfare and Rehabilitation Sciences. Written informed consent was obtained from all participants. Sixty (n = 60) subjects (20 male, 40 female, mean ± SD age: 38 ± 4 years) have participated. Subjects were recruited from patients referring to the physiotherapy clinic of University of Social Welfare and Rehabilitation Sciences. Participants were included if they had a history of chronic, nonspecific neck pain of more than 3 months as well as a palpable tenderness on cervical joints. Patients were excluded if they had any history of cervical spine surgery, any cervical trauma (e.g., whiplash), any neurological signs, taking medications or any physiotherapy treatment, or had participated in a neck or shoulder exercise programs within last six months. The sample size was based on previous studies detecting differences of 20% in cross sectional area (CSA) or thickness of multifidus muscle between healthy subjects and patients with chronic neck pain [12]. Assuming a standard deviation of 10%, an alpha level of 0.05, and a desired power of 90%, the sample size generated was 30 subjects in each group. Therefore, the study had sufficient power to detect the effect of exercise intervention on cervical muscles dimensions. The participants were randomly assigned into either a CCF group or a CF group through block style randomization sequence. 2.2. Outcome measures 2.2.1. Muscle dimensions An US device (ultrasonix, medical corp., ES500 Canada) with a 12.5 MHz linear array and 38 mm foot print probe was used. For LC muscle size measurement, the subjects were positioned supine, 2 cm
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2.3. Treatment interventions All subjects performed their exercise program under supervision of an experienced physical therapist 3 times per week for 10 weeks. Maximum duration of any exercise session was 30 min. Subjects were advised not to receive any other specific intervention for their pain along with the interventions of the current study. All subjects were asked to perform exercises 3 times per day during the study. It was reminded that the exercises should be performed with no pain.
Fig. 1. Ultrasonography image of sternoclidomastoid (SCM) and longus colli (LC).
below the thyroid cartilage was marked by a marker, and the image was captured at this level (about C6) in the relaxed state of the muscle [13]. Anterior posterior dimension (APD), lateral dimension (LD) and CSA were measured 3 times and the average was reported. APD of the sternocleidomastoid (SCM) muscle was also measured 3 times in the same position of the patient and transducer (Fig. 1). The mean data was used for further analysis. 2.2.2. Pain intensity and functional disability The mean intensity of neck pain was assessed with an 11-point numerical pain rate scale (NPRS, 0: no current pain, 10: maximum pain) [14]. Cleland et al reported that the minimal detectable change (MDC) and the minimal clinically important difference (MCID) were 1.3 and 2.1 points, respectively for patients with neck pain (15). The neck disability index (NDI) which is a widely accepted disability questionnaire was used to assess functional disability. It contains 10 items, 7 related to activities of daily living, 2 related to pain, and 1 item related to concentration. Each item is scored from 0 to 5. The numeric score for each item is summed for a total score varying from 0 to 50, where higher scores reflect greater disability. The NDI has shown to be reliable and valid for patients with neck pain and has shown a MDC of 20% for patients with neck pain [15]. In present study, NDI was measured using validated Iranian version of related questionnaire [16].
2.3.1. CCF intervention The CCF program was performed according to the protocol described by O’Leary et al. [11]. This exercise seems to activate deep anterior muscles of the cervical spine including LC and longus capitis rather than the superficial flexors, such as SCM and anterior scalene [11]. The exercise is a low load training in order to target specifically deep cervical flexors rather than the neck flexors as a whole which may occur in a high load training of neck flexors. An air-filled pressure sensor held under neck monitored the flattening of the cervical lordosis which caused by longus colli contraction (Fig. 2a). By the feedback from the pressure sensor, subjects were trained to gradually reach 5 pressure targets in 2 mmHg increments from a baseline of 20 mmHg to the final level of 30 mmHg. Subjects were asked to gently nod their head as they were saying “yes”. The maximum pressure level that the subjects could hold steadily without involvement of superficial muscles and without quick jerky CCF movement, was monitored and considered as patients’ level of deep muscle performance. An experienced and qualified physical therapist monitored the contraction and prohibited applying contraction of superficial muscles in all stages of the test using observation and palpation. Training was started at the target level achieved by the subject without any contribution of the superficial flexors (SCM, hyoid and anterior scalene). The subjects were asked to perform a slow and controlled CCF. They trained to increase ranges of CCF using feedback from the pressure sensor placed behind their neck. For each pressure target level, the duration of the contraction was 10 seconds followed by 10 seconds rest, and the subject had to perform the contraction 10 times. Then the subject could progress to the next level.
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(a)
(b)
Fig. 2. Two types of exercise program, a: Craniocervical flexion, b: Cervical flexion (Adopted from O’Leary et al. [11]).
2.3.2. CF intervention In a supine and comfortable resting position of the head, patients were asked to lift up their head through full range of motion as much as possible without any discomfort or reproducing of the symptoms. The upper cervical spine was placed in neutral position and the movement had to be performed slowly through the range (Fig. 2b). The exercise program was divided into two separate stages. According to the recommendation of previous studies for untrained subjects, the duration of the first and second stage was set for 2 and 8 weeks, respectively [11]. For every subject, 12 repetition maximum (RM) was identified at the first session, progressed gradually to 15 RM and this level was maintained for the reminder of the stage. In stage 2, patients performed 3 sets of 15 repetitions of the initial 12 RM, 3 times per day. One minute interval between sets was applied. If patients could perform the exercise easily, then weighted sandbags were added to their forehead with 0.5 kg increments. If the patients were unable to perform exercise easily then the load on neck flexors was reduced by allowing the patients to perform the task with the upper body (trunk and neck) inclined up from the horizontal. In this situation the subjects could do the required repetitions of the movements.
groups using independent t-tests for continuous data and 2 tests of independence for categorical data. Separated 2 × 2 mixed model ANOVAs with time (prepost) as a within-subject variable and group (CCF training and CF training) as the between-subject variable was used to examine the effects of interventions on pain, disability and each muscle dimension outcome. The hypothesis of interest was the Group * Time interaction at -level equal to 0.05. To enable comparison of effect sizes, standardized mean differences (SMDs) was calculated by dividing mean score differences between experimental and control groups by the pooled standard deviation. P values lower than 0.05 were considered as statistically significant for all analyses.
3. Results Sixty patients (20 male, 40 female; mean age: 36 ± 4 years; height: 164 ± 6 cm; weight: 66 ± 10 kg) with mechanical neck pain who met the inclusion/exclusion criteria and agreed to participate, were randomly assigned into either a CCF training group (n = 30) or a CF training group (n = 30). All patients have completed the study. No significant differences were found for baseline clinical features and muscle dimensions between the two groups (Table 1).
2.4. Data analysis 3.1. Changes in neck muscles dimensions Statistical analysis was conducted with the SPSS package version 18.0. Mean, standard deviation and/or 95% confidence intervals for each outcome measure are presented. The Kolmogorov-Smirnov test showed a normal distribution of the data (P > 0.05 in all instances). Baseline features were compared between
After 10 weeks of intervention, significant group * time interactions were found in all muscle outcomes: the CCF training group demonstrated a significant increase in LC muscle dimensions including CSA (F = 28.235; P < 0.001), width (F = 9.863; P = 0.003)
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Table 1 Baseline characteristics of patients in the two groups Craniocervical flexion exercise Mean ± SD Range 36.8 ± 3.5 27–40 3.33 ± 3.22 0.33–12 4.97 ± 2.39 1.5–9.8 33.27 ± 11.4 14–56
Age (y) Pain duration (y) Neck pain intensity VAS (0–10 cm) Neck pain disability (0–100%)
Cervical flexion exercise Mean ± SD Range 35.7 ± 5 19–40 3.32 ± 3.22 0.25–12 5.07 ± 2.15 1.7–9.8 33.2 ± 15 4–68
Table 2 Neck exercise and muscle dimensions in patients with chronic neck pain
Pain intensity Functional disability SCM thickness (mm) LCM CSA cm2 APD mm LD mm
Pre exercise Mean (SD) 4.97 ± 2.39 33.27 ± 11.4 9.300 (2.01) 0.786 (0.04) 8.150 (0.28) 13.89 (0.45)
CCF Post exercise Mean (SD) 2.27 ± 1.51 15.20 ± 9.16 9.300 (1.89) 0.953 (0.05) 9.216 (0.56) 14.810 (0.52)
Diff (mean) 2.70 ± 1.63 18.07 ± 10.2 0.000 0.167 ± 0.02 1.06 ± 0.45 0.92 ± 0.17
Pre exercise Mean (SD) 5.07 ± 2.15 33.2 ± 15.1 9.400 (1.86) 0.790 (0.04) 8.146 (0.25) 13.893 (0.48)
CF Post exercise Mean (SD) 2.75 ± 1.41 19.01 ± 10.1 10.133 (1.77) 0.884 (0.05) 8.900 (0.32) 14.436 (0.46)
Diff (mean) 2.32 ± 1.19 14.2 ± 11.2 0.733 0.094 0.754 0.543
Abbreviations: CCF (craniocervical flexion), CF (cervical flexion), Diff (difference), SD (standard deviation). 1
LCCSA1
0.953
0.95
LCCSA2 0.884
0.9
LCAPD2
9.5
9.216 8.9
9
0.85 0.8
LCAPD1
10
0.79
0.786
8.5
0.75
8.15
8.146
8
0.7
7.5
0.65
7
0.6 0.55
6.5
0.5
C CF
CF
Fig. 3. Pre intervention and post intervention cross sectional area of longus colli.
and thickness (F = 37.634; P < 0.001) compared with CF (Figs 3–5; Table 2), whereas the CF group demonstrated a significant increase (F = 26.167; P < 0.001) in SCM thickness as compared to the CCF group (Fig. 6; Table 2). Between-groups effect sizes were large for SCM thickness (SMD: 1.05) and moderate for LC muscle dimensions (0.65 < SMD < 0.50) 3.2. Changes of pain and disability The 2 × 2 ANOVA demonstrated no significant group * time interactions for neck pain intensity (F = 1.508, P = 0.308) and disability (F = 1.986, P = 0.164): neck pain intensity and disability decreased
6
CCF
CF
Fig. 4. Pre intervention and post intervention anterior and posterior dimensions of longus colli.
similarly in both groups (Table 2). Between-groups effect sizes were small for both outcomes (SMD: 0.35).
4. Discussion The results of this study demonstrated that exercise programs targeting deep cervical flexor muscles (CCF program) increased LC muscle dimensions and CF program tended to increased SCM muscle thickness in individuals with mechanical neck pain. In addition, the exercise programs were equally effective on pain and disability.
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16
LCLD1 14.81
15 14
LCLD2 14.436
13.89
13.893
13 12 11 10
C CF
CF
Fig. 5. Pre intervention and post intervention lateral dimensions of longuss colli.
Fig. 6. Change in sternoclidomastoid (SCM) muscle after CF exercise.
Considering the high recurrence rate of neck pain and the stabilizing function of deep cervical flexors [17], specific exercise programs may have a prohibiting effect on recurrence rate of cervical pain. To the best of the authors’ knowledge, the present study is the first of its kind to assess the effect of specific exercise regimes on the muscle size of the deep cervical flexors utilizing US. It was found that CCF exercise program increased LC muscle dimensions including CSA, thickness and width, whereas the CF exercise program increased SCM thickness only in pa-
tients suffering from mechanical neck pain. It seems that in CCF program the main focus is initially on recruitment of deep cervical flexors, whereas in CF program the patient learns to lift head which leads to general activation of neck flexors including deep and superficial muscles. Evidences emphasize on the importance of deep cervical muscle sleeve for stability of cervical spine [18, 19]. Falla et al. reported deep cervical flexor muscles dysfunction in patients with chronic neck pain. In fact, pain itself and fear of pain may tend to different recruitment pattern of anterior or posterior deep and superficial muscle groups [20]. Abnormal recruitment may result in inhibition of deep layer and hyperactivity of superficial layer. Decreased activity of deep flexors in patients with neck pain may result in diminished support and control of the cervical spine joints and compensatory increase of superficial muscles including anterior scalene and SCM [21]. While EMG findings in neck pain have shown impaired co-ordination of deep and superficial cervical flexors [20] and increased latency of muscle action, studies utilizing US and MRI have demonstrated decreased dimension of the muscles [7,22]. Therefore, it seems that both muscle dimension and motor control may be affected in patients with neck pain. Some studies have pointed out the disturbance of deep and superficial muscles co-ordination resulted in hyperactivity of superficial muscles in patients with neck pain (e.g. [23]). Previous study conducted on comparison of LC muscle dimensions between healthy subjects and patients with chronic neck pain showed that CSA and thickness of LC in patients group were smaller than that of healthy controls [22]. It appears that response to exercise program is greater in weak muscles. Long term training of muscles may alter the recruitment pattern via the neuromuscular control units and repetition of a specific task lead to adaptive changes of the spinal muscles. This idea was supported by Conley et al. [24]. In an MRI study, it was reported that the size of SCM and splenius capitis muscles significantly increased after a period of resistive head and neck extension exercise [24]. After 10 weeks of exercise, similar decreases on pain and perceived disability were found in both groups. Different studies have shown significant relationship between increasing muscle strength and decreasing pain intensity in patients with neck pain [17, 22,23,25]. Also light cervical proprioception exercises showed immediate pain reduction following intervention [26].
K. Javanshir et al. / The effect of different exercise programs on CF muscles dimensions
Several studies demonstrated that different exercise regimes may tend to reduced neck pain immediately post intervention compared with a control group (e.g. [27–29]). In addition, other studies have also indicated that exercise programs reduced disability in patients with neck pain. Falla et al. reported similar reduction in disability after the same two different exercise protocol (strength-endurance training and CCF) on 58 females suffering from chronic neck pain [25]. In another study conducted by Ylinen [29], investigating the effect of different exercise programs, similar immediate decreases in disability was found. The results of the present study are in accordance with previous data, confirming that both exercise programs are equally effective for reducing pain and disability in patients with neck pain. According to the results of the present study, it seems that recruitment of neck flexor muscles in normal pattern within the CCF group resulted in strengthening of deep flexor muscles and increasing of muscle dimensions. The changes of LC muscle in present study may be indicative of an altered capacity of this muscle sleeve to better support the cervical spine in patients suffering from chronic neck pain.
5. Conclusion The results demonstrated that the exercise program targeting the deep neck flexors (CCF program) increased LC muscle dimensions including CSA, thickness and width, whereas the exercise generally recruiting neck flexors (CF program) increased SCM thickness in patients suffering from mechanical neck pain. In addition, exercise programs targeting either the deep cervical flexors or generally deep and superficial muscles were equally effective on pain and disability in individuals with neck pain.
Ethical approval The study was given ethical approval from Medical Ethics Board, at the University of Social Welfare and Rehabilitation Sciences, Tehran, Iran References [1]
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Acknowledgment The authors acknowledge all subjects participating in this study.
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Conflict of interest There is no conflict of interest in this study. Meanwhile, the paper was not previously presented or published in any form anywhere.
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