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Respiratory weakness in patients with chronic neck pain
Manual Therapy 18 (2013) 248e253
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Manual Therapy journal homepage: www.elsevier.com/math
Original article
Respiratory weakness in patients with chronic neck pain Zacharias Dimitriadis a, b, *, Eleni Kapreli a, Nikolaos Strimpakos a, b, Jacqueline Oldham b a b
Physiotherapy Department, Technological Educational Institute (TEI) of Lamia, 3rd km Old National Road Lamia-Athens, 35100 Lamia, Greece Manchester Academic Health Sciences Centre, The University of Manchester, Oxford Road, Manchester M13 9PL, UK
a r t i c l e i n f o
a b s t r a c t
Article history: Received 1 April 2012 Received in revised form 24 October 2012 Accepted 30 October 2012
Respiratory muscle strength is one parameter that is currently proposed to be affected in patients with chronic neck pain. This study was aimed at examining whether patients with chronic neck pain have reduced respiratory strength and with which neck pain problems their respiratory strength is associated. In this controlled cross-sectional study, 45 patients with chronic neck pain and 45 healthy well-matched controls were recruited. Respiratory muscle strength was assessed through maximal mouth pressures. The subjects were additionally assessed for their pain intensity and disability, neck muscle strength, endurance of deep neck flexors, neck range of movement, forward head posture and psychological states. Paired t-tests showed that patients with chronic neck pain have reduced Maximal Inspiratory (MIP) (r ¼ 0.35) and Maximal Expiratory Pressures (MEP) (r ¼ 0.39) (P < 0.05). Neck muscle strength (r > 0.5), kinesiophobia (r < 0.3) and catastrophizing (r < 0.3) were significantly associated with maximal mouth pressures (P < 0.05), whereas MEP was additionally negatively correlated with neck pain and disability (r < 0.3, P < 0.05). Neck muscle strength was the only predictor that remained as significant into the prediction models of MIP and MEP. It can be concluded that patients with chronic neck pain present weakness of their respiratory muscles. This weakness seems to be a result of the impaired global and local muscle system of neck pain patients, and psychological states also appear to have an additional contribution. Clinicians are advised to consider the respiratory system of patients with chronic neck pain during their usual assessment and appropriately address their treatment. Ó 2012 Elsevier Ltd. All rights reserved.
Keywords: Chronic neck pain Maximal expiratory pressure Maximal inspiratory pressure Respiration
1. Introduction Chronic neck pain is one of the most frequent musculoskeletal complaints and can lead to adaptive musculoskeletal and motor control changes in cervical region and related structures (Falla and Farina, 2008; Jull et al., 2008a). Although neck pain is predominantly considered and treated in clinical practice as a neuromusculoskeletal problem, the close anatomical connection of the cervical region with the thoracic spine in parallel with their musculoskeletal and neural connection have led some researchers to believe that neck pain may lead to associated changes in thoracic spine and rib cage and consequential changes in pulmonary function (Kapreli et al., 2008). Cervical spine studies have shown that muscle strength and endurance (Chiu and Lo, 2002; Harris et al., 2005), cervical mobility (Rix and Bagust, 2001), head posture (Lau et al., 2009) and cervical proprioception (Cheng et al., 2010) are all affected in patients with
* Corresponding author. Physiotherapy Department, Technological Educational Institute (TEI) of Lamia, 3rd km Old National Road Lamia-Athens, 35100 Lamia, Greece. Tel.: þ30 22310 60176. E-mail address: [email protected] (Z. Dimitriadis). 1356-689X/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.math.2012.10.014
chronic neck pain, whereas abnormal psychological states namely anxiety, depression, kinesiophobia and catastrophizing may also be present (Leino and Magni, 1993; Hill et al., 2007; Mantyselka et al., 2010). It has been recently theorized that all of these parameters can have their own unique contribution for the development of respiratory dysfunction or abnormalities in patients with chronic neck pain (Kapreli et al., 2008) and preliminarily supported by a previous pilot study (Kapreli et al., 2009). Changes in cervical mobility, head posture and dysfunction of local and global muscle system are believed that lead to changes in forceelength curves, muscle imbalances and segmental instability (Gossman et al., 1982; Comerford and Mottram, 2001; Key et al., 2008) potentially affecting the function of thoracic cage and rib cage mechanics (Kapreli et al., 2008). This dysfunction might be more apparent during inspiration as the common muscles of cervical region and respiration (sternocleidomastoid, scaleni and trapezius) are all inspiratory in function (Palastanga et al., 2002). Furthermore, the existence of psychological factors such as kinesiophobia might also lead to movement avoidance further contributing to the dysfunction of cervical muscles and consequentially to the potential changes in rib cage mechanics (Kapreli et al., 2008). These changes in rib cage biomechanics could lead to associated changes of respiratory muscles altering their forceelength curves
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and force production abilities (Gossman et al., 1982; Kapreli et al., 2008). Piloting findings support this belief as patients with chronic neck pain have been found to present reduction in their maximal mouth pressures (Kapreli et al., 2009). However, existent literature provides no other known evidence about the strength of respiratory muscles in patients with chronic neck pain. Furthermore, the association of respiratory strength with the common musculoskeletal and psychological manifestations of patients with chronic neck pain remains completely unexplored. The examination of the respiratory strength and its association with the known manifestations of neck pain could lead to a better understanding of the changes occurring due to neck pain and to improvement of the usual assessment and treatment provided in these patients. Given the above, this study was aimed at investigating the possible existence of respiratory weakness in chronic neck pain patients and the correlations among the aforementioned factors. The hypotheses of the present study were that: H0: Patients with chronic neck pain have no different maximal inspiratory and expiratory pressures from healthy controls. and H0: Maximal inspiratory and expiratory pressures of patients with chronic neck pain are not correlated with their musculoskeletal (forward head posture, strength of neck muscles, endurance of deep neck flexors, cervical range of movement, pain intensity) and psychological (anxiety, depression, catastrophizing, kinesiophobia) manifestations.
2. Methods 2.1. Sample In this cross-sectional study, 45 patients with chronic neck pain and 45 healthy gender-, age-, height- and weight-matched controls were conveniently recruited. Patients were included if they had pain for at least 6 months with pain complaints at least once a week and were between 18 and 65 year old. Patients with spinal or chest surgeries, smoking history, traumatic cervical injuries, acute or chronic neuromusculoskeletal pain in any other non-related body area, serious obesity (Body Mass Index (BMI) >40), clinical abnormalities of the thoracic cage or vertebral column, occupational industrial exposures, serious comorbidities (neurological, neuromuscular, cardiorespiratory, psychiatric and musculoskeletal disorders), diabetes mellitus and/or malignancies were excluded from the study. The same eligibility criteria were applied for the healthy control group. Healthy controls were individually matched with neck pain patients in terms of gender, age (5 years), height (10 cm) and weight (10%). All the participants were assessed at the cardiorespiratory lab of the Physiotherapy Department, Technological Educational Institute (TEI) of Lamia, Lamia, Greece during the 2009e2010 years. All the subjects had to sign an informed consent before their participation to this study. The study was approved by the Ethics Committee of the Department of Physiotherapy, School of Health and Caring Professions, TEI Lamia, Greece and the University of Manchester Ethics Committee. 2.2. Procedure Maximal Inspiratory Pressure (MIP) and Maximal Expiratory Pressure (MEP) were assessed in a randomized order from a standing position (Fig. 1) with a portable mouth pressure meter
Fig. 1. Positioning for assessing maximal mouth pressures.
(microRPM, Micro Medical Limited, Rochester, Kent, England) and the accompanying PUMA PC software [Intraclass Correlation Coefficient (ICC) ¼ 0.81e0.83, Standard Error of Measurement (SEM) ¼ 12e14 cmH2O] (Dimitriadis et al., 2011). After a short demonstration of the procedure, the volunteers were asked to perform 5 maximal inspiratory and expiratory efforts with an at least 30-s interval between the trials. During the measurement of maximal mouth pressures the participants were asked to close firmly their mouth around the flanged mouthpiece. A noseclip was fitted to avoid any air leak. A small piece of tape was placed on the mouth pressure meter monitor in order for the participants to be blind to their performance. The MEP was assessed after asking the participants to inhale as much as possible and then to exhale maximally against the resistance of the gauge for at least 1 s. The MIP was recorded after asking the participants to expire as much as possible and then to inhale maximally against the resistance of the gauge for at least 1 s. The participants were verbally encouraged throughout the procedure for maximal performance. The best of the inspiratory and expiratory efforts were recorded as the MIP and MEP respectively. The maximal voluntary isometric strength of neck flexors and extensors was assessed in a randomized order from the Neutral Head Position (NHP) after a short warm-up period. The measurements were performed in standing position with a custom-made
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isometric neck dynamometer using a previously described procedure (Strimpakos et al., 2004). High reliability values with small measurement error have been also previously published (ICC ¼ 0.9e0.96, SEM ¼ 12.6e20.8 N) (Strimpakos et al., 2004). The craniocervical flexion test was used for assessing the endurance of deep neck flexors. Details about the procedure and reliability values are provided by previous publications (ICC ¼ 0.91) (Jull et al., 2008a, 2008b; Arumugam et al., 2011). The measurements were performed from a crook lying position with a pressure biofeedback device (Stabilizer, Chattanooga, USA), which was placed behind participants’ neck. The device was initially inflated to a baseline pressure of 20 mmHg. The participants had to successively perform 3 10-s holds of a head nodding action at each of the 5 pressure levels (22 mmHg, 24 mmHg, 26 mmHg, 28 mmHg and 30 mmHg). Participants’ deep neck flexors were considered fatigued when pressure decrease at the pressure sensor, apparent activation of the superficial neck flexors or a jerky action during holding of the pressure level were observed. The endurance of deep neck flexors of each participant was considered the maximal pressure that the participant was able to keep steady for three 10-s holds without any other substitution strategy. Cervical Range of Movement (ROM) of all neck movements was assessed by using the Zebris ultrasound-based motion analysis system (Zebris Meditchnic GmbH, Isny, Germany) from a standing position, based on instructions provided by a previously published paper (Strimpakos et al., 2005). After calibrating the Zebris in order for the NHP to be defined equal to 0 , the participants were asked to perform three repetitions for each cervical movement. For each cervical movement the best trial was accepted. The procedure has been found very reliable with small measurement error (ICC ¼ 0.73e0.86, SEM ¼ 6.5e8.5 ) (Strimpakos et al., 2005). The Forward Head Posture (FHP) was assessed through the craniovertebral angle (CVA), the angle between the line extending from the tragus of the ear to the 7th cervical vertebra (C7) spinous process and the horizontal line through C7. For this purpose three lateral photographs were obtained after asking the participants to focus their vision on a predetermined reference point at the height of their eyes. The photographs were obtained by using a digital colour camera (HDR-SR11E, Sony, Belgium), and the values were calculated by using a 3-D drawing software (Auto-CAD 2000, Autodesk Inc., San Raphael, CA). The mean of the three CVAs was used for data analysis. The procedure has been previously reported as very reliable (ICC ¼ 0.88) (Raine and Twomey, 1997). A number of questionnaires were given to participants including Visual Analogue Scales for assessing current and usual neck pain intensity (Price et al., 1983), Neck Disability Index for assessing pain-induced disability (Trouli et al., 2008) and the Baecke Questionnaire of Habitual Physical Activity for assessing physical activity level (Baecke et al., 1982). Furthermore, the cross-cultural validated Hospital Anxiety and Depression Scale (Georgoudis and Oldham, 2001), Tampa Scale for Kinesiophobia (Georgoudis et al., 2007) and Pain Catastrophizing Scale (Argyra et al., 2006) were completed in a randomized order to reduce any potential bias and ordering effects. 2.3. Data analysis Pearson correlation coefficients and paired t-tests were used for examining the correlations between the variables and the differences between the groups, respectively. A backward stepwise multiple regression analysis (removal ¼ 0.1) was performed for MIP and MEP. The strength of neck extensors, endurance of deep neck flexors, sagittal ROM, FHP, usual pain intensity, anxiety, depression, kinesiophobia and catastrophizing were selected to be the predictors of these models. When data were missing, the individual with
Fig. 2. Differences in Maximal Inspiratory Pressure (MIP) and Maximal Expiratory Pressure (MEP) between patients with chronic neck pain (grey colour) and healthy controls (white colour).
his/her matched participant were removed from the analysis of this variable. One patient had missing data on left rotation and left lateral flexion ROM due to software problems, 1 patient had missing data on craniocervical flexion test because he had forgotten his glasses and could not read the feedback from the pressure sensor and 1 healthy control had missing data on FHP as the hairclip was broken and was not possible to free the cervical area. The significance level was defined equal to 0.05. Statistical Package of Social Sciences (SPSS, version 17) was used for all data analysis. 3. Results The patients with chronic neck pain [32 females, age: 35.9(14.5) years, height: 165.8(9.2) cm, weight: 71.6(16) kg, BMI: 25.9(4.5), physical activity: 7.9(1.3)] did not differ significantly from the healthy matched controls [32 females, age: 35.4(14) years, height: 167.1(8.7) cm, weight: 72.3(15.2) kg, BMI: 25.8(4.4), physical activity: 7.6(1.4)] in age, height, weight, BMI and physical activity level (P > 0.05). The patients of the study were predominantly of mild to moderate neck pain intensity [VAS: 45.5(18.8) mm] and of mild disability [HADS: 10.6(5.2)] and had pain chronicity of 69.6(57.6) months. Their pain intensity during the measurements was 19.3(19.1) mm. The patients were also found to have weak neck extensors (P < 0.05) and trend for weak neck flexors. They were also presented with reduced mobility in all cervical movement planes and impaired deep neck flexors (P < 0.05). However, their FHP was similar to the control group and they were not more anxious or depressed (P > 0.05). Patients with chronic neck pain had a significant 13.8% and 15.4% reduction in their MIP and MEP respectively (P < 0.05) (Fig. 2), but the MIP/MEP ratio was not significantly affected (P > 0.05) (Table 1). Table 1 Differences in maximal mouth pressures between patients with chronic neck pain and healthy controls.
MIP (cmH2O) MEP (cmH2O) MIP/MEP
Neck pain M (SD)
Controls M (SD)
Mean difference (95% CI)
r
86.9 (31.2) 107.36 (43.3) 0.85 (0.22)
100.8 (34.5) 126.9 (43.1) 0.81 (0.17)
13.9 (25.1, 2.7)* 19.5 (33.6, 5.5)** 0.03 (0.05, 0.12)
0.35 0.39 0.12
*P < 0.05, **P < 0.01 MIP: Maximal Inspiratory Pressure, MEP: Maximal Expiratory Pressure.
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MIP was significantly correlated with strength of neck flexors (r ¼ 0.7, P < 0.001) and extensors (r ¼ 0.62, P < 0.001), kinesiophobia (r ¼ 0.43, P < 0.01) and catastrophizing (r ¼ 0.3, P < 0.05). MEP was significantly correlated with strength of neck flexors (r ¼ 0.69, P < 0.001) and extensors (r ¼ 0.66, P < 0.001), usual pain intensity (r ¼ 0.33, P < 0.05), Neck Disability Index (NDI) (r ¼ 0.35, P < 0.05), kinesiophobia (r ¼ 0.4, P < 0.05) and
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catastrophizing (r ¼ 0.36, P < 0.05) (Fig. 3). All the other correlations were not significant and of small effect size (r < 0.3, P > 0.05). The regression analysis showed that the assumption of independent errors, homoscedasticity, linearity and normally distributed errors had been met. Multicollinearity was not found to be of concern and no influential outliers were recognized. The models
Fig. 3. Correlations between maximal mouth pressures [maximal inspiratory pressure (black dots, solid line) and maximal expiratory pressure (white dots, dashed line)] and strength of neck extensors (upper left), strength of neck flexors (upper right), pain intensity (middle left), disability (middle right), kinesiophobia (bottom left) and catastrophizing (bottom right) (NDI: Neck Disability Index, TSK: Tampa Scale for Kinesiophobia, PCK: Pain Catastrophizing Scale).
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revealed that strength of neck extensors is the only significant common predictor of MIP and MEP. However, the MIP model also included kinesiophobia and the MEP model also included FHP as predictors (Table 2). The multiple correlation coefficients and the generalizability of the prediction models of MIP (R ¼ 0.66, R2 ¼ 0.44, adjusted R2 ¼ 0.41) and MEP (R ¼ 0.7, R2 ¼ 0.49, adjusted R2 ¼ 0.46) were satisfactory. 4. Discussion This study was designed to investigate the potential existence of respiratory weakness in patients with chronic neck pain and its associations with neck pain manifestations. According to the findings, patients with chronic neck pain have reduced strength of respiratory muscles. Neck muscle strength, kinesiophobia and catastrophizing are significantly correlated with respiratory muscle strength, whereas pain intensity and disability are additionally associated with strength of expiratory muscles. However, only the strength of neck muscles remains as significant predictor of respiratory weakness when all the neck pain complaints are put together into a regression model. The results of the study are supported by the preliminary findings by Kapreli et al. (2009) where a 21.5% drop of MIP and 16.5% drop of MEP were also observed. The fact that the MIP/MEP ratio was not different suggests that the two respiratory indices were similarly reduced in patients with chronic neck pain. This fact implies that the reduction in respiratory muscle strength cannot be attributed only to the common function of sternocleidomastoid, scaleni and trapezius in neck movement and inspiration, since in this case inspiratory pressures could be more affected. Thus, the origins of this weakness should be the result of additional physical and psychological mechanisms. Strength of neck muscles was found to be the deficit which is mostly associated with strength of respiratory muscles. Although this association could be attributed to a generalized weakness of patients with chronic neck pain, the same physical activity levels of the two groups does not justify such a notion. Thus, this association could be mainly based on the affected kinetic control of the cervical area. Patients with chronic neck pain were found to have reduced performance of their global and local muscles. Dysfunction of these muscles is believed to lead to reduced respiratory performance mainly because of a) the common function of sternocleidomastoid, trapezius and scaleni on cervical movement and inspiration (Palastanga et al., 2002; Legrand et al., 2003), b) changes in forcee length curves and muscles imbalances (Gossman et al., 1982), c) segmental instability of the cervical spine (Comerford and Mottram, 2001) which might be also observed in thoracic spine because of muscles such as longus colli which attach in both areas Table 2 Regression models for the prediction of Maximal Inspiratory Pressure (MIP) and Maximal Expiratory Pressure (MEP). This table presents the beta values (B) with their 95% Confidence Intervals (95% CI) and their Standard Error (SE B) as well as the standardized beta values (b) for the prediction of MIP and MEP in patients with chronic neck pain. B (95% CI) MIP prediction Constant Strength of neck extensors Kinesiophobia MEP prediction Constant Strength of neck extensors Forward head posture **P < 0.01, ***P < 0.001.
92.14 (45.13, 139.14)*** 1.98 (1.05, 2.91)*** 1.06 (2.2, 0.09) 133.98 (46.82, 221.14)** 3.53 (2.37, 4.69)*** 1.67 (3.5, 0.12)
SE B
b
23.27 0.46 0.57
0.54 0.23
43.16 0.57 0.89
0.7 0.21
(Palastanga et al., 2002) and d) impairment of neck proprioceptors (Boyd-Clark et al., 2002) rendering more difficult for the patients to find the optimal alignment of their spine (Key et al., 2008). These changes have been proposed to lead to adapted kinetic and kinematic patterns of rib cage, changing the forceelength relationships of the associated respiratory muscles and consequentially leading to alteration of their contraction patterns (Kapreli et al., 2008). These mechanical changes of respiratory muscles may influence their force production abilities and can lead to a permanent respiratory weakness due to plastic changes (Gajdosik, 2001; Bruton, 2002). The existence of psychological states seems to play an additional role contributing to this respiratory weakness. Kinesiophobia may directly lead to reduced respiratory strength due to poorer performance during the pulmonary function testing (Ruppel, 2009). However, its role seems to be rather indirect through a further deconditioning of the neck muscles because of prolonged neck movement avoidance (Kapreli et al., 2008). Limited neck movement can lead to deconditioning of neck muscles and adaptive changes (Gajdosik, 2001; Bruton, 2002) further affecting the local and global muscles and consequentially respiratory function. Interestingly, pain intensity and disability were found to be correlated only with MEP. If the respiratory weakness observed in patients with neck pain was mostly dependent on the common function of sternocleidomastoid, scaleni and trapezius in cervical movement and respiration, MIP would be expected to have a stronger association with this respiratory weakness. This fact reveals that respiratory muscle weakness in patients with chronic neck pain cannot be mainly attributed to the common function of these muscles on both neck movement and inspiration and highlights that this weakness is a multidimensional dysfunction where causes should be also sought in combination with the biomechanical and psychological mechanisms of other neck pain problems. An interesting trend was also observed in the regression models as it was found that FHP can negatively predict MEP. This means that an increase in FHP is associated with improved respiratory strength. Although this association seems to be strange, it has been also noted in a previous pilot study (Kapreli et al., 2009). Okuro et al. (2011) have also reported that children with forward head posture present increased MIP and MEP. Forward head posture can be adopted by patients with poor breathing as an attempt to increase airflow and improve respiratory function (Perri and Halford, 2004; Okuro et al., 2011). Thus, FHP in patients with chronic neck pain can be viewed not only as a maladaptive posture, but it might be also a compensatory mechanism for improving respiratory function. In comparison to normative data established by Evans and Whitelaw (2009), patients with chronic neck pain had 5.5% reduction in their inspiratory and 4.1% reduction in their expiratory muscle strength (Evans and Whitelaw, 2009). However, in this study patients’ respiratory strength was compared with the respiratory strength of healthy matched-controls and was found to present a higher decrease (13.8%e15.4%). This difference can be attributed to the fact that the latter percentages derived from comparison with a similar sample of healthy participants rather than from predicted models based on a different population. Although there is no objective cut-off point for defining muscle weakness, the decrease in respiratory strength of neck patients does not exceed 20% which is the percentage proposed by the American Thoracic Society/European Respiratory Society for defining considerable decline in muscle strength (American Thoracic Society/European Respiratory Society, 2002). However, even though this fact reveals that the respiratory weakness of patients with chronic neck pain cannot be considered as
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pathological, there is an obvious dysfunction of respiratory muscles which needs clinical attention. Provided that the sample of patients used in this study was predominantly of mild neck pain and disability, it could be stipulated that the observed respiratory weakness may be more pronounced in patients of more severe condition and requires further investigation. The respiratory weakness observed in patients with chronic neck pain can importantly influence the clinical scientists as it is accompanied by important clinical implications about the usual treatment of chronic neck pain. Based on the findings of this study, it can be suggested that the respiratory function should be also included into assessment and treatment of patients with chronic neck pain. However, future studies should also examine the effectiveness of additional respiratory exercises as complementary to the usual treatment of patients with chronic neck pain. Electromyographic studies can enhance the knowledge about the activation patterns of muscles related with cervical and respiratory function in patients with chronic neck pain. Studies by using optoelectronic plethysmography can also offer a better understanding of respiratory function and respiratory kinematics in these patients contributing to more suitable designs of therapeutic protocols. 5. Conclusions Chronic neck pain does not seem to be a condition related only with neuromusculoskeletal and psychological manifestations, but it appears to have more dimensions. Respiratory function of patients with chronic neck pain can be also affected as they present with weakness of their respiratory muscles. Cervical muscle dysfunction and psychological influences appear to be the factors that are mostly associated with this respiratory dysfunction. These conclusions suggest the incorporation of assessment and rehabilitation of respiratory function into the usual clinical approaches used for patients with chronic neck pain. This can lead to changes in clinical reasoning with potentially more optimal therapeutic outcomes for these chronic pain sufferers. Acknowledgements We would like to thank the participants for the willingness to participate in this study, Ms Lamprini Komnianou for technical assistance and Dr Steve Roberts for statistical advice. References American Thoracic Society/European Respiratory Society. ATS/ERS statement on respiratory muscle testing. American Journal of Respiratory and Critical Care Medicine 2002;166(4):518e624. Argyra E, Georgoudis G, Chatzidimitriou A, Siafaka I, Vadalouka A. Cognitive assessment of Greek pain patients: validation of the pain catastrophing scale. Palliative Medicine 2006;20:232. Arumugam A, Mani R, Raja K. Interrater reliability of the craniocervical flexion test in asymptomatic individualsea cross-sectional study. Journal of Manipulative and Physiological Therapeutics 2011;34(4):247e53. Baecke JA, Burema J, Frijters JE. A short questionnaire for the measurement of habitual physical activity in epidemiological studies. American Journal of Clinical Nutrition 1982;36(5):936e42. Boyd-Clark LC, Briggs CA, Galea MP. Muscle spindle distribution, morphology, and density in longus colli and multifidus muscles of the cervical spine. Spine 2002; 27(7):694e701. Bruton A. Muscle plasticity: response to training and detraining. Physiotherapy 2002;88(7):398e408. Cheng CH, Wang JL, Lin JJ, Wang SF, Lin KH. Position accuracy and electromyographic responses during head reposition in young adults with chronic neck pain. Journal of Electromyography and Kinesiology 2010;20(5):1014e20.
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Manual Therapy journal homepage: www.elsevier.com/math
Original article
Respiratory weakness in patients with chronic neck pain Zacharias Dimitriadis a, b, *, Eleni Kapreli a, Nikolaos Strimpakos a, b, Jacqueline Oldham b a b
Physiotherapy Department, Technological Educational Institute (TEI) of Lamia, 3rd km Old National Road Lamia-Athens, 35100 Lamia, Greece Manchester Academic Health Sciences Centre, The University of Manchester, Oxford Road, Manchester M13 9PL, UK
a r t i c l e i n f o
a b s t r a c t
Article history: Received 1 April 2012 Received in revised form 24 October 2012 Accepted 30 October 2012
Respiratory muscle strength is one parameter that is currently proposed to be affected in patients with chronic neck pain. This study was aimed at examining whether patients with chronic neck pain have reduced respiratory strength and with which neck pain problems their respiratory strength is associated. In this controlled cross-sectional study, 45 patients with chronic neck pain and 45 healthy well-matched controls were recruited. Respiratory muscle strength was assessed through maximal mouth pressures. The subjects were additionally assessed for their pain intensity and disability, neck muscle strength, endurance of deep neck flexors, neck range of movement, forward head posture and psychological states. Paired t-tests showed that patients with chronic neck pain have reduced Maximal Inspiratory (MIP) (r ¼ 0.35) and Maximal Expiratory Pressures (MEP) (r ¼ 0.39) (P < 0.05). Neck muscle strength (r > 0.5), kinesiophobia (r < 0.3) and catastrophizing (r < 0.3) were significantly associated with maximal mouth pressures (P < 0.05), whereas MEP was additionally negatively correlated with neck pain and disability (r < 0.3, P < 0.05). Neck muscle strength was the only predictor that remained as significant into the prediction models of MIP and MEP. It can be concluded that patients with chronic neck pain present weakness of their respiratory muscles. This weakness seems to be a result of the impaired global and local muscle system of neck pain patients, and psychological states also appear to have an additional contribution. Clinicians are advised to consider the respiratory system of patients with chronic neck pain during their usual assessment and appropriately address their treatment. Ó 2012 Elsevier Ltd. All rights reserved.
Keywords: Chronic neck pain Maximal expiratory pressure Maximal inspiratory pressure Respiration
1. Introduction Chronic neck pain is one of the most frequent musculoskeletal complaints and can lead to adaptive musculoskeletal and motor control changes in cervical region and related structures (Falla and Farina, 2008; Jull et al., 2008a). Although neck pain is predominantly considered and treated in clinical practice as a neuromusculoskeletal problem, the close anatomical connection of the cervical region with the thoracic spine in parallel with their musculoskeletal and neural connection have led some researchers to believe that neck pain may lead to associated changes in thoracic spine and rib cage and consequential changes in pulmonary function (Kapreli et al., 2008). Cervical spine studies have shown that muscle strength and endurance (Chiu and Lo, 2002; Harris et al., 2005), cervical mobility (Rix and Bagust, 2001), head posture (Lau et al., 2009) and cervical proprioception (Cheng et al., 2010) are all affected in patients with
* Corresponding author. Physiotherapy Department, Technological Educational Institute (TEI) of Lamia, 3rd km Old National Road Lamia-Athens, 35100 Lamia, Greece. Tel.: þ30 22310 60176. E-mail address: [email protected] (Z. Dimitriadis). 1356-689X/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.math.2012.10.014
chronic neck pain, whereas abnormal psychological states namely anxiety, depression, kinesiophobia and catastrophizing may also be present (Leino and Magni, 1993; Hill et al., 2007; Mantyselka et al., 2010). It has been recently theorized that all of these parameters can have their own unique contribution for the development of respiratory dysfunction or abnormalities in patients with chronic neck pain (Kapreli et al., 2008) and preliminarily supported by a previous pilot study (Kapreli et al., 2009). Changes in cervical mobility, head posture and dysfunction of local and global muscle system are believed that lead to changes in forceelength curves, muscle imbalances and segmental instability (Gossman et al., 1982; Comerford and Mottram, 2001; Key et al., 2008) potentially affecting the function of thoracic cage and rib cage mechanics (Kapreli et al., 2008). This dysfunction might be more apparent during inspiration as the common muscles of cervical region and respiration (sternocleidomastoid, scaleni and trapezius) are all inspiratory in function (Palastanga et al., 2002). Furthermore, the existence of psychological factors such as kinesiophobia might also lead to movement avoidance further contributing to the dysfunction of cervical muscles and consequentially to the potential changes in rib cage mechanics (Kapreli et al., 2008). These changes in rib cage biomechanics could lead to associated changes of respiratory muscles altering their forceelength curves
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and force production abilities (Gossman et al., 1982; Kapreli et al., 2008). Piloting findings support this belief as patients with chronic neck pain have been found to present reduction in their maximal mouth pressures (Kapreli et al., 2009). However, existent literature provides no other known evidence about the strength of respiratory muscles in patients with chronic neck pain. Furthermore, the association of respiratory strength with the common musculoskeletal and psychological manifestations of patients with chronic neck pain remains completely unexplored. The examination of the respiratory strength and its association with the known manifestations of neck pain could lead to a better understanding of the changes occurring due to neck pain and to improvement of the usual assessment and treatment provided in these patients. Given the above, this study was aimed at investigating the possible existence of respiratory weakness in chronic neck pain patients and the correlations among the aforementioned factors. The hypotheses of the present study were that: H0: Patients with chronic neck pain have no different maximal inspiratory and expiratory pressures from healthy controls. and H0: Maximal inspiratory and expiratory pressures of patients with chronic neck pain are not correlated with their musculoskeletal (forward head posture, strength of neck muscles, endurance of deep neck flexors, cervical range of movement, pain intensity) and psychological (anxiety, depression, catastrophizing, kinesiophobia) manifestations.
2. Methods 2.1. Sample In this cross-sectional study, 45 patients with chronic neck pain and 45 healthy gender-, age-, height- and weight-matched controls were conveniently recruited. Patients were included if they had pain for at least 6 months with pain complaints at least once a week and were between 18 and 65 year old. Patients with spinal or chest surgeries, smoking history, traumatic cervical injuries, acute or chronic neuromusculoskeletal pain in any other non-related body area, serious obesity (Body Mass Index (BMI) >40), clinical abnormalities of the thoracic cage or vertebral column, occupational industrial exposures, serious comorbidities (neurological, neuromuscular, cardiorespiratory, psychiatric and musculoskeletal disorders), diabetes mellitus and/or malignancies were excluded from the study. The same eligibility criteria were applied for the healthy control group. Healthy controls were individually matched with neck pain patients in terms of gender, age (5 years), height (10 cm) and weight (10%). All the participants were assessed at the cardiorespiratory lab of the Physiotherapy Department, Technological Educational Institute (TEI) of Lamia, Lamia, Greece during the 2009e2010 years. All the subjects had to sign an informed consent before their participation to this study. The study was approved by the Ethics Committee of the Department of Physiotherapy, School of Health and Caring Professions, TEI Lamia, Greece and the University of Manchester Ethics Committee. 2.2. Procedure Maximal Inspiratory Pressure (MIP) and Maximal Expiratory Pressure (MEP) were assessed in a randomized order from a standing position (Fig. 1) with a portable mouth pressure meter
Fig. 1. Positioning for assessing maximal mouth pressures.
(microRPM, Micro Medical Limited, Rochester, Kent, England) and the accompanying PUMA PC software [Intraclass Correlation Coefficient (ICC) ¼ 0.81e0.83, Standard Error of Measurement (SEM) ¼ 12e14 cmH2O] (Dimitriadis et al., 2011). After a short demonstration of the procedure, the volunteers were asked to perform 5 maximal inspiratory and expiratory efforts with an at least 30-s interval between the trials. During the measurement of maximal mouth pressures the participants were asked to close firmly their mouth around the flanged mouthpiece. A noseclip was fitted to avoid any air leak. A small piece of tape was placed on the mouth pressure meter monitor in order for the participants to be blind to their performance. The MEP was assessed after asking the participants to inhale as much as possible and then to exhale maximally against the resistance of the gauge for at least 1 s. The MIP was recorded after asking the participants to expire as much as possible and then to inhale maximally against the resistance of the gauge for at least 1 s. The participants were verbally encouraged throughout the procedure for maximal performance. The best of the inspiratory and expiratory efforts were recorded as the MIP and MEP respectively. The maximal voluntary isometric strength of neck flexors and extensors was assessed in a randomized order from the Neutral Head Position (NHP) after a short warm-up period. The measurements were performed in standing position with a custom-made
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isometric neck dynamometer using a previously described procedure (Strimpakos et al., 2004). High reliability values with small measurement error have been also previously published (ICC ¼ 0.9e0.96, SEM ¼ 12.6e20.8 N) (Strimpakos et al., 2004). The craniocervical flexion test was used for assessing the endurance of deep neck flexors. Details about the procedure and reliability values are provided by previous publications (ICC ¼ 0.91) (Jull et al., 2008a, 2008b; Arumugam et al., 2011). The measurements were performed from a crook lying position with a pressure biofeedback device (Stabilizer, Chattanooga, USA), which was placed behind participants’ neck. The device was initially inflated to a baseline pressure of 20 mmHg. The participants had to successively perform 3 10-s holds of a head nodding action at each of the 5 pressure levels (22 mmHg, 24 mmHg, 26 mmHg, 28 mmHg and 30 mmHg). Participants’ deep neck flexors were considered fatigued when pressure decrease at the pressure sensor, apparent activation of the superficial neck flexors or a jerky action during holding of the pressure level were observed. The endurance of deep neck flexors of each participant was considered the maximal pressure that the participant was able to keep steady for three 10-s holds without any other substitution strategy. Cervical Range of Movement (ROM) of all neck movements was assessed by using the Zebris ultrasound-based motion analysis system (Zebris Meditchnic GmbH, Isny, Germany) from a standing position, based on instructions provided by a previously published paper (Strimpakos et al., 2005). After calibrating the Zebris in order for the NHP to be defined equal to 0 , the participants were asked to perform three repetitions for each cervical movement. For each cervical movement the best trial was accepted. The procedure has been found very reliable with small measurement error (ICC ¼ 0.73e0.86, SEM ¼ 6.5e8.5 ) (Strimpakos et al., 2005). The Forward Head Posture (FHP) was assessed through the craniovertebral angle (CVA), the angle between the line extending from the tragus of the ear to the 7th cervical vertebra (C7) spinous process and the horizontal line through C7. For this purpose three lateral photographs were obtained after asking the participants to focus their vision on a predetermined reference point at the height of their eyes. The photographs were obtained by using a digital colour camera (HDR-SR11E, Sony, Belgium), and the values were calculated by using a 3-D drawing software (Auto-CAD 2000, Autodesk Inc., San Raphael, CA). The mean of the three CVAs was used for data analysis. The procedure has been previously reported as very reliable (ICC ¼ 0.88) (Raine and Twomey, 1997). A number of questionnaires were given to participants including Visual Analogue Scales for assessing current and usual neck pain intensity (Price et al., 1983), Neck Disability Index for assessing pain-induced disability (Trouli et al., 2008) and the Baecke Questionnaire of Habitual Physical Activity for assessing physical activity level (Baecke et al., 1982). Furthermore, the cross-cultural validated Hospital Anxiety and Depression Scale (Georgoudis and Oldham, 2001), Tampa Scale for Kinesiophobia (Georgoudis et al., 2007) and Pain Catastrophizing Scale (Argyra et al., 2006) were completed in a randomized order to reduce any potential bias and ordering effects. 2.3. Data analysis Pearson correlation coefficients and paired t-tests were used for examining the correlations between the variables and the differences between the groups, respectively. A backward stepwise multiple regression analysis (removal ¼ 0.1) was performed for MIP and MEP. The strength of neck extensors, endurance of deep neck flexors, sagittal ROM, FHP, usual pain intensity, anxiety, depression, kinesiophobia and catastrophizing were selected to be the predictors of these models. When data were missing, the individual with
Fig. 2. Differences in Maximal Inspiratory Pressure (MIP) and Maximal Expiratory Pressure (MEP) between patients with chronic neck pain (grey colour) and healthy controls (white colour).
his/her matched participant were removed from the analysis of this variable. One patient had missing data on left rotation and left lateral flexion ROM due to software problems, 1 patient had missing data on craniocervical flexion test because he had forgotten his glasses and could not read the feedback from the pressure sensor and 1 healthy control had missing data on FHP as the hairclip was broken and was not possible to free the cervical area. The significance level was defined equal to 0.05. Statistical Package of Social Sciences (SPSS, version 17) was used for all data analysis. 3. Results The patients with chronic neck pain [32 females, age: 35.9(14.5) years, height: 165.8(9.2) cm, weight: 71.6(16) kg, BMI: 25.9(4.5), physical activity: 7.9(1.3)] did not differ significantly from the healthy matched controls [32 females, age: 35.4(14) years, height: 167.1(8.7) cm, weight: 72.3(15.2) kg, BMI: 25.8(4.4), physical activity: 7.6(1.4)] in age, height, weight, BMI and physical activity level (P > 0.05). The patients of the study were predominantly of mild to moderate neck pain intensity [VAS: 45.5(18.8) mm] and of mild disability [HADS: 10.6(5.2)] and had pain chronicity of 69.6(57.6) months. Their pain intensity during the measurements was 19.3(19.1) mm. The patients were also found to have weak neck extensors (P < 0.05) and trend for weak neck flexors. They were also presented with reduced mobility in all cervical movement planes and impaired deep neck flexors (P < 0.05). However, their FHP was similar to the control group and they were not more anxious or depressed (P > 0.05). Patients with chronic neck pain had a significant 13.8% and 15.4% reduction in their MIP and MEP respectively (P < 0.05) (Fig. 2), but the MIP/MEP ratio was not significantly affected (P > 0.05) (Table 1). Table 1 Differences in maximal mouth pressures between patients with chronic neck pain and healthy controls.
MIP (cmH2O) MEP (cmH2O) MIP/MEP
Neck pain M (SD)
Controls M (SD)
Mean difference (95% CI)
r
86.9 (31.2) 107.36 (43.3) 0.85 (0.22)
100.8 (34.5) 126.9 (43.1) 0.81 (0.17)
13.9 (25.1, 2.7)* 19.5 (33.6, 5.5)** 0.03 (0.05, 0.12)
0.35 0.39 0.12
*P < 0.05, **P < 0.01 MIP: Maximal Inspiratory Pressure, MEP: Maximal Expiratory Pressure.
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MIP was significantly correlated with strength of neck flexors (r ¼ 0.7, P < 0.001) and extensors (r ¼ 0.62, P < 0.001), kinesiophobia (r ¼ 0.43, P < 0.01) and catastrophizing (r ¼ 0.3, P < 0.05). MEP was significantly correlated with strength of neck flexors (r ¼ 0.69, P < 0.001) and extensors (r ¼ 0.66, P < 0.001), usual pain intensity (r ¼ 0.33, P < 0.05), Neck Disability Index (NDI) (r ¼ 0.35, P < 0.05), kinesiophobia (r ¼ 0.4, P < 0.05) and
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catastrophizing (r ¼ 0.36, P < 0.05) (Fig. 3). All the other correlations were not significant and of small effect size (r < 0.3, P > 0.05). The regression analysis showed that the assumption of independent errors, homoscedasticity, linearity and normally distributed errors had been met. Multicollinearity was not found to be of concern and no influential outliers were recognized. The models
Fig. 3. Correlations between maximal mouth pressures [maximal inspiratory pressure (black dots, solid line) and maximal expiratory pressure (white dots, dashed line)] and strength of neck extensors (upper left), strength of neck flexors (upper right), pain intensity (middle left), disability (middle right), kinesiophobia (bottom left) and catastrophizing (bottom right) (NDI: Neck Disability Index, TSK: Tampa Scale for Kinesiophobia, PCK: Pain Catastrophizing Scale).
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revealed that strength of neck extensors is the only significant common predictor of MIP and MEP. However, the MIP model also included kinesiophobia and the MEP model also included FHP as predictors (Table 2). The multiple correlation coefficients and the generalizability of the prediction models of MIP (R ¼ 0.66, R2 ¼ 0.44, adjusted R2 ¼ 0.41) and MEP (R ¼ 0.7, R2 ¼ 0.49, adjusted R2 ¼ 0.46) were satisfactory. 4. Discussion This study was designed to investigate the potential existence of respiratory weakness in patients with chronic neck pain and its associations with neck pain manifestations. According to the findings, patients with chronic neck pain have reduced strength of respiratory muscles. Neck muscle strength, kinesiophobia and catastrophizing are significantly correlated with respiratory muscle strength, whereas pain intensity and disability are additionally associated with strength of expiratory muscles. However, only the strength of neck muscles remains as significant predictor of respiratory weakness when all the neck pain complaints are put together into a regression model. The results of the study are supported by the preliminary findings by Kapreli et al. (2009) where a 21.5% drop of MIP and 16.5% drop of MEP were also observed. The fact that the MIP/MEP ratio was not different suggests that the two respiratory indices were similarly reduced in patients with chronic neck pain. This fact implies that the reduction in respiratory muscle strength cannot be attributed only to the common function of sternocleidomastoid, scaleni and trapezius in neck movement and inspiration, since in this case inspiratory pressures could be more affected. Thus, the origins of this weakness should be the result of additional physical and psychological mechanisms. Strength of neck muscles was found to be the deficit which is mostly associated with strength of respiratory muscles. Although this association could be attributed to a generalized weakness of patients with chronic neck pain, the same physical activity levels of the two groups does not justify such a notion. Thus, this association could be mainly based on the affected kinetic control of the cervical area. Patients with chronic neck pain were found to have reduced performance of their global and local muscles. Dysfunction of these muscles is believed to lead to reduced respiratory performance mainly because of a) the common function of sternocleidomastoid, trapezius and scaleni on cervical movement and inspiration (Palastanga et al., 2002; Legrand et al., 2003), b) changes in forcee length curves and muscles imbalances (Gossman et al., 1982), c) segmental instability of the cervical spine (Comerford and Mottram, 2001) which might be also observed in thoracic spine because of muscles such as longus colli which attach in both areas Table 2 Regression models for the prediction of Maximal Inspiratory Pressure (MIP) and Maximal Expiratory Pressure (MEP). This table presents the beta values (B) with their 95% Confidence Intervals (95% CI) and their Standard Error (SE B) as well as the standardized beta values (b) for the prediction of MIP and MEP in patients with chronic neck pain. B (95% CI) MIP prediction Constant Strength of neck extensors Kinesiophobia MEP prediction Constant Strength of neck extensors Forward head posture **P < 0.01, ***P < 0.001.
92.14 (45.13, 139.14)*** 1.98 (1.05, 2.91)*** 1.06 (2.2, 0.09) 133.98 (46.82, 221.14)** 3.53 (2.37, 4.69)*** 1.67 (3.5, 0.12)
SE B
b
23.27 0.46 0.57
0.54 0.23
43.16 0.57 0.89
0.7 0.21
(Palastanga et al., 2002) and d) impairment of neck proprioceptors (Boyd-Clark et al., 2002) rendering more difficult for the patients to find the optimal alignment of their spine (Key et al., 2008). These changes have been proposed to lead to adapted kinetic and kinematic patterns of rib cage, changing the forceelength relationships of the associated respiratory muscles and consequentially leading to alteration of their contraction patterns (Kapreli et al., 2008). These mechanical changes of respiratory muscles may influence their force production abilities and can lead to a permanent respiratory weakness due to plastic changes (Gajdosik, 2001; Bruton, 2002). The existence of psychological states seems to play an additional role contributing to this respiratory weakness. Kinesiophobia may directly lead to reduced respiratory strength due to poorer performance during the pulmonary function testing (Ruppel, 2009). However, its role seems to be rather indirect through a further deconditioning of the neck muscles because of prolonged neck movement avoidance (Kapreli et al., 2008). Limited neck movement can lead to deconditioning of neck muscles and adaptive changes (Gajdosik, 2001; Bruton, 2002) further affecting the local and global muscles and consequentially respiratory function. Interestingly, pain intensity and disability were found to be correlated only with MEP. If the respiratory weakness observed in patients with neck pain was mostly dependent on the common function of sternocleidomastoid, scaleni and trapezius in cervical movement and respiration, MIP would be expected to have a stronger association with this respiratory weakness. This fact reveals that respiratory muscle weakness in patients with chronic neck pain cannot be mainly attributed to the common function of these muscles on both neck movement and inspiration and highlights that this weakness is a multidimensional dysfunction where causes should be also sought in combination with the biomechanical and psychological mechanisms of other neck pain problems. An interesting trend was also observed in the regression models as it was found that FHP can negatively predict MEP. This means that an increase in FHP is associated with improved respiratory strength. Although this association seems to be strange, it has been also noted in a previous pilot study (Kapreli et al., 2009). Okuro et al. (2011) have also reported that children with forward head posture present increased MIP and MEP. Forward head posture can be adopted by patients with poor breathing as an attempt to increase airflow and improve respiratory function (Perri and Halford, 2004; Okuro et al., 2011). Thus, FHP in patients with chronic neck pain can be viewed not only as a maladaptive posture, but it might be also a compensatory mechanism for improving respiratory function. In comparison to normative data established by Evans and Whitelaw (2009), patients with chronic neck pain had 5.5% reduction in their inspiratory and 4.1% reduction in their expiratory muscle strength (Evans and Whitelaw, 2009). However, in this study patients’ respiratory strength was compared with the respiratory strength of healthy matched-controls and was found to present a higher decrease (13.8%e15.4%). This difference can be attributed to the fact that the latter percentages derived from comparison with a similar sample of healthy participants rather than from predicted models based on a different population. Although there is no objective cut-off point for defining muscle weakness, the decrease in respiratory strength of neck patients does not exceed 20% which is the percentage proposed by the American Thoracic Society/European Respiratory Society for defining considerable decline in muscle strength (American Thoracic Society/European Respiratory Society, 2002). However, even though this fact reveals that the respiratory weakness of patients with chronic neck pain cannot be considered as
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pathological, there is an obvious dysfunction of respiratory muscles which needs clinical attention. Provided that the sample of patients used in this study was predominantly of mild neck pain and disability, it could be stipulated that the observed respiratory weakness may be more pronounced in patients of more severe condition and requires further investigation. The respiratory weakness observed in patients with chronic neck pain can importantly influence the clinical scientists as it is accompanied by important clinical implications about the usual treatment of chronic neck pain. Based on the findings of this study, it can be suggested that the respiratory function should be also included into assessment and treatment of patients with chronic neck pain. However, future studies should also examine the effectiveness of additional respiratory exercises as complementary to the usual treatment of patients with chronic neck pain. Electromyographic studies can enhance the knowledge about the activation patterns of muscles related with cervical and respiratory function in patients with chronic neck pain. Studies by using optoelectronic plethysmography can also offer a better understanding of respiratory function and respiratory kinematics in these patients contributing to more suitable designs of therapeutic protocols. 5. Conclusions Chronic neck pain does not seem to be a condition related only with neuromusculoskeletal and psychological manifestations, but it appears to have more dimensions. Respiratory function of patients with chronic neck pain can be also affected as they present with weakness of their respiratory muscles. Cervical muscle dysfunction and psychological influences appear to be the factors that are mostly associated with this respiratory dysfunction. These conclusions suggest the incorporation of assessment and rehabilitation of respiratory function into the usual clinical approaches used for patients with chronic neck pain. This can lead to changes in clinical reasoning with potentially more optimal therapeutic outcomes for these chronic pain sufferers. Acknowledgements We would like to thank the participants for the willingness to participate in this study, Ms Lamprini Komnianou for technical assistance and Dr Steve Roberts for statistical advice. References American Thoracic Society/European Respiratory Society. ATS/ERS statement on respiratory muscle testing. American Journal of Respiratory and Critical Care Medicine 2002;166(4):518e624. Argyra E, Georgoudis G, Chatzidimitriou A, Siafaka I, Vadalouka A. Cognitive assessment of Greek pain patients: validation of the pain catastrophing scale. Palliative Medicine 2006;20:232. Arumugam A, Mani R, Raja K. Interrater reliability of the craniocervical flexion test in asymptomatic individualsea cross-sectional study. Journal of Manipulative and Physiological Therapeutics 2011;34(4):247e53. Baecke JA, Burema J, Frijters JE. A short questionnaire for the measurement of habitual physical activity in epidemiological studies. American Journal of Clinical Nutrition 1982;36(5):936e42. Boyd-Clark LC, Briggs CA, Galea MP. Muscle spindle distribution, morphology, and density in longus colli and multifidus muscles of the cervical spine. Spine 2002; 27(7):694e701. Bruton A. Muscle plasticity: response to training and detraining. Physiotherapy 2002;88(7):398e408. Cheng CH, Wang JL, Lin JJ, Wang SF, Lin KH. Position accuracy and electromyographic responses during head reposition in young adults with chronic neck pain. Journal of Electromyography and Kinesiology 2010;20(5):1014e20.
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