Electromyographic Activity of the Cervical Flexor Muscles in Patients With Temporomandibular Disorders While Performing the Craniocervical Flexion

Test: A Cross-Sectional Study Susan Armijo-Olivo, Rony Silvestre, Jorge Fuentes, Bruno R. da Costa, Inae C. Gadotti, Sharon Warren, Paul W. Major, Norman M.R. Thie and David J. Magee PHYS THER. 2011; 91:1184-1197. Originally published online June 9, 2011 doi: 10.2522/ptj.20100233 The online version of this article, along with updated information and services, can be found online at: http://ptjournal.apta.org/content/91/8/1184 Collections This article, along with others on similar topics, appears in the following collection(s): Anatomy and Physiology: Musculoskeletal System Injuries and Conditions: Head and Jaw Tests and Measurements To submit an e-Letter on this article, click here or click on "Submit a response" in the right-hand menu under "Responses" in the online version of this article. Sign up here to receive free e-mail alerts

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Research Report
Electromyographic Activity of the Cervical Flexor Muscles in Patients With Temporomandibular Disorders While Performing the Craniocervical Flexion Test: A Cross-Sectional Study
Susan Armijo-Olivo, Rony Silvestre, Jorge Fuentes, Bruno R. da Costa, Inae C. Gadotti, Sharon Warren, Paul W. Major, Norman M.R. Thie, David J. Magee
S. Armijo-Olivo, BScPT, MSc, PhD, Department of Physical Therapy, Faculty of Rehabilitation Medicine, and Alberta Research Centre for Health Evidence, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, Canada. Mailing address: Department of Physical Therapy, Rehabilitation Research Centre, Faculty of Rehabilitation Medicine, University of Alberta, 350 Corbett Hall, Edmonton, Alberta, Canada T6G 2G4. Address all correspondence to Dr Armijo-Olivo at: sla4@ualberta.ca or susanarmijo@gmail.com. R. Silvestre, BScPT, MSc, Research Center of Human Movement, Mayor University, Santiago, Chile. J. Fuentes, BSc, MScRS, Rehabilitation Research Centre, Faculty of Rehabilitation Medicine, University of Alberta, and Department of Physical Therapy, Catholic University of Maule, Talca, Chile. B.R. da Costa, BScPT, MSc, Institute of Social & Preventive Medicine, University of Bern, Bern, Switzerland. I.C. Gadotti, BScPT, MScPT, PhD, Department of Physical Therapy, College of Nursing and Health Sciences, Florida International University, Miami, Florida. S. Warren, PhD, Faculty of Rehabilitation Medicine, University of Alberta. Author information continues on next page.

Background. Most patients with temporomandibular disorders (TMD) have been shown to have cervical spine dysfunction. However, this cervical dysfunction has been evaluated only qualitatively through a general clinical examination of the cervical spine. Purpose. The purpose of this study was to determine whether patients with TMD
had increased activity of the supercial cervical muscles when performing the craniocervical exion test (CCFT) compared with a control group of individuals who were healthy.

Design. A cross-sectional study was conducted. Methods. One hundred fty individuals participated in this study: 47 were
healthy, 54 had myogenous TMD, and 49 had mixed TMD. All participants performed the CCFT. Data for electromyographic activity of the sternocleidomastoid (SCM) and anterior scalene (AS) muscles were collected during the CCFT for all participants. A 3-way mixed-design analysis of variance for repeated measures was used to evaluate the differences in EMG activity for selected muscles while performing the CCFT under 5 incremental levels. Effect size values were calculated to evaluate the clinical relevance of the results.

Results. Although there were no statistically signicant differences in electromyographic activity in the SCM or AS muscles during the CCFT in patients with mixed and myogenous TMD compared with the control group, those with TMD tended to have increased activity of the supercial cervical muscles.

Limitations. The results obtained in this research are applicable for the group of individuals who participated in this study under the protocols used. They could potentially be applied to people with TMD having characteristics similar to those of the participants of this study. Conclusion. This information may give clinicians insight into the importance of
evaluation and possible treatment of the deep neck exors in patients with TMD. However, future research should test the effectiveness of this type of program through a randomized controlled trial in people with TMD in order to determine the real value of treating this type of impairment in this population.

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Cervical Flexor Activity and Temporomandibular Disorders

P.W. Major, DDS, MSc, FRCD(c), School of Dentistry, University of Alberta. N.M.R. Thie, BSc, MSc, DDS, TMD/Orofacial Pain Graduate Program, School of Dentistry, University of Alberta. D.J. Magee, PhD, Department of Physical Therapy, Faculty of Rehabilitation Medicine, University of Alberta. [Armijo-Olivo S, Silvestre R, Fuentes J, et al. Electromyographic activity of the cervical exor muscles in patients with temporomandibular disorders while performing the craniocervical exion test: a cross-sectional study. Phys Ther. 2011;91:1184 1197.] 2011 American Physical Therapy Association Published Ahead of Print: June 9, 2011 Accepted: April 8, 2011 Submitted: July 14, 2010

emporomandibular disorders (TMD) are the most prevalent category of nondental chronic pain conditions in the orofacial region. These disorders are characterized by pain affecting the masticatory muscles, the temporomandibular joint (TMJ), and related structures.1 Temporomandibular disorders interfere with daily activities and can signicantly affect quality of life, diminishing patients capacity for work and ability to interact with their social environment.2 It has been calculated that approximately $2 billion has been spent in the United States due to TMD direct care.3 Patients with TMD have shown high levels of unemployment and decreased work effectiveness.4 In a large, population-based, crosssectional study, it was shown that TMD chronic pain had an individual impact and burden similar to that of back pain, severe headache, and chest and abdominal pain.5 In a recent study,6 women comprised more than 70% of the patients having TMD, and the ratio between women and men was 2.4:1 for arthralgia, 2.5:1 for osteoarthritis, 3.4:1 for myofascial pain, and 5.1:1 for TMJ disk displacement.6 The literature supports the fact that women are more sensitive to pain conditions, reporting more severe pain, more frequent pain, and pain of longer duration than men.714 In addition, women are more prompt in seeking help than men. Therefore, it seems that women more commonly have TMD and may seek care for TMD pain more often than men.3 Temporomandibular disorders have commonly been associated with symptoms affecting the head and neck region, such as headache, cervical spine dysfunction,15,16 and altered head and cervical posture.1721 It has been reported that pain in the cervical musculoskeletal tissues may be referred to cranial

structures, including the jaw muscles22,23; thus, a connection between cervical muscle dysfunction and jaw symptoms could exist.24 27 Additionally, animal studies have revealed considerable convergence of craniofacial and cervical afferents in the trigeminocervical nucleus and upper cervical nociceptive neurons.28 31 All of this evidence has been the theoretical foundation of pain localization and referral and of neuromuscular adaptations in the cervical and orofacial regions.3234 However, to date, no research has demonstrated a cause-and-effect relationship. As stated above, TMD are categorized as musculoskeletal disorders that commonly involve the cervical region. Other musculoskeletal disorders associated with the cervical region, such as neck pain, cervicogenic headache, and whiplashassociated disorders, are characterized by abnormal function of the cervical muscles.3537 However, it is unknown whether people with TMD have these muscular alterations. Given the close connection between the cervical spine and the orofacial region, knowledge about impairments in the cervical spine in people with TMD could help clinicians focus their efforts on properly evaluating and treating these impairments. Previous work has shown that gross changes in strength (force-generating capacity) and endurance have been observed in cervical-related disorders. However, according to Jull et al36 and Falla and Farina,38 ner changes in cervical muscular activity of the cervical spine are present. Reduced activation of deep cervical muscles, augmented supercial activity of the sternocleidomastoid (SCM) and anterior scalene (AS) muscles, changes in feedforward activation, reduced capacity to relax the cervical muscles, and prolonged muscle activity following voluntary contraction could lead to a compromise in
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Cervical Flexor Activity and Temporomandibular Disorders the control of the cervical spine and consequently lead to pain and dysfunction.36 Study of these muscular alterations has gained attention in the last few years, as exercises addressing these motor control alterations have had good results in patients with cervical involvement.39 41 Therefore, the assessment and treatment of muscular impairments is considered a key element in the management of cervicalassociated disorders. Because TMD have been considered part of the cervical-associated disorders, it may be plausible that similar features could be seen in this patient group. Knowledge about these features would be useful for clinicians treating patients with TMD. However, studies of muscular impairments in patients with TMD are lacking. Cervical dysfunction in patients with TMDs has been evaluated only qualitatively through a general clinical examination of the cervical spine. Most of the studies have looked at cervical spine signs and symptoms in people with TMD, but they have not investigated any motor alterations in a quantitative way. For example, de Wijer and colleagues27,42 concluded that symptoms of the stomatognathic system overlap in patients with TMD and cervical spine disorders and that symptoms of the cervical spine overlap in the same group of patients. Visscher et al25 found that patients with chronic TMD more often had cervical spine pain than those without this disorder. Stiesch-Scholz et al43 found that asymptomatic functional disorders of the cervical spine occurred more frequently in patients with internal derangement of the TMJ than in a control group. The presence of tender points in the cervical spine and shoulder girdle in patients with the same diagnosis was more common, especially in upper segments of the cervical spine, compared with a control group of individuals who were healthy. Furthermore, a recent systematic review44 showed that exercises for the neck that also were used to improve neck and head posture decreased symptoms in patients with TMD. However, the systematic review found that details of the exercises and exercise programs (ie, type of exercise, dosage, and frequency) were lacking, as well as a clear underlying mechanism of why these exercises, directed toward to the neck, improved TMD symptoms. Based on the above information, it was evident that a more quantitative evaluation of the motor activity of the cervical muscles through electromyographic (EMG) assessment, looking at performance patterns of the cervical musculature activity in patients with TMD, could assist in clarifying the role of the cervical muscles involvement in the symptoms of these patients. Additionally, this evaluation could open an area of study aimed at treating these alterations through improvement of motor control of the cervical muscles in patients with TMD. The main objective of this study was to determine, through EMG evaluation, whether patients with myogenous TMD and mixed TMD had altered muscle activity (ie, higher EMG activity) of the supercial cervical muscles (SCM and AS) when performing the CCFT compared with a control group of individuals who were healthy. The secondary objectives of this study were: (1) to determine whether there was an association between the performance of the cervical exor muscles during the 5 stages of the CCFT and neck disability and jaw disability and (2) to determine whether there was an association between level of chronic disability in patients with TMD based on the Research Diagnostic Criteria for Temporomandibular
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The Bottom Line What do we already know about this topic?

Cervical spine dysfunction has been reported to be associated with temporomandibular disorders (TMD). Temporomandibular disorders also are commonly associated with other symptoms affecting the head and neck region such as headache, ear-related symptoms, and altered head and cervical posture. However, no study has investigated the presence of cervical muscle impairments using electromyography.

What new information does this study offer?

The results of this study may give clinicians insight into the importance of the evaluation and possible treatment of the deep neck exors in patients with TMD. However, randomized clinical trials are necessary to determine the effectiveness of an exercise program targeting the deep neck exors in these patients.

If youre a patient, what might these ndings mean for you?

If you have a TMD, these ndings may help your physical therapist evaluate your condition. This evaluation would include an examination of the cervical musculature as well as the TMD.

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Cervical Flexor Activity and Temporomandibular Disorders Disorders45 (RDC/TMD) (Chronic Pain Grade Disability Questionnaire for TMD), pain intensity, duration of complaint, and performance of the cervical exor muscles during the 5 stages of the CCFT. Table 1.
Descriptive Statistics of Height, Weight, and Age and Clinical Characteristics of Participants by Groupa
Variable Height (cm) Group Myogenous TMD (n 54) Healthy (n 47) Mixed TMD (n 49) Weight (kg) Myogenous TMD Healthy Mixed TMD Age (y) Myogenous TMD Healthy Mixed TMD Duration of complaint (y) Myogenous TMD Healthy Mixed TMD Pain intensity (0100 mm) Myogenous TMD Healthy Mixed TMD Neck Disability Index (050 points) Myogenous TMD Healthy Mixed TMD Jaw Function Scale (1050 points) Myogenous TMD Healthy Mixed TMD X 165.1 165.0 166.3 64.1
b

SD 5.1 6.8 5.9 9.9 12.7 15.9 9.0 7.5 8.3 6.4 0.0 6.4 17.3 0.0 16.1 5.5 1.6 6.8 6.6 0.4 7.1

Method
Design A cross-sectional conducted. study was

64.3b 72.1c 31.4 28.3 31.3 6.5c 0.0 8.3c 45.3c 0.0 49.0c 10.5c 1.6 12.6c 18.6b,c 10.1 22.7c .05. .05.

Participants A convenience sample of patients who attended the TMD/Orofacial Pain Clinic at the School of Dentistry, Faculty of Medicine and Dentistry, University of Alberta, and students and staff at the University of Alberta who were healthy was recruited for this study. The sample size for this study was calculated based on a repeated-measures analysis of variance (ANOVA) following the guidelines established by Stevens (with .05, 0.20, power 80%, and effect size 0.57).46 A minimum of 40 participants per group was needed. The inclusion and exclusion criteria for the individuals who were healthy and the patients with TMD have been described elsewhere.47,48 In brief, people who were healthy were included if they were women between the ages of 18 and 50 years16 and they did not have a history of musculoskeletal pain, TMD symptoms, neurological disease, systemic disease, or mental illness that could interfere with the outcomes. Patients with TMD were included if they were women between 18 and 50 years of age, had pain in the masticatory muscles or TMJ of at least 3 months duration, and had a moderate or severe baseline pain score ( 30 mm) on a 100-mm visual analog scale (VAS).49 Patients were classied as having myogenous TMD based on the classication Ia and Ib of Dworkin and LeResche.45 In addition, they had to have pain upon palpation in at least 3 of the 12 musAugust 2011
a b c

TMD temporomandibular disorders. Signicantly different compared with participants with mixed TMD at Signicantly different compared with participants who were healthy at

cular points proposed by Fricton and Schiffman.50 52 Patients were diagnosed as having mixed TMD if they complained of muscular symptoms in addition to TMJ symptoms such as painful clicking, crepitation, or pain in the TMJ at rest or during function53 and during a compression test.54 A total 168 individuals were assessed for inclusion in this study. A total of 18 individuals were excluded. The main reasons for exclusion were: not totally healthy (n 9), older than 50 years of age (n 2), having a neurological disease (n 1), having cancer (n 1), and having a pain score lower than 30 mm on the VAS (n 5). One hundred fty participants provided data for this study: 47 were healthy,

54 had myogenous TMD, and 49 had mixed TMD. The general demographics for each group and the clinical characteristics of the participants are displayed in Table 1. There were no signicant differences in age and height in the sample (P .05). However, weight was signicantly different between participants with mixed TMD and those with myogenous TMD (mean difference 8.0 kg, 95% condence interval [CI] 1.9 to 14.2; P .006) and between participants with mixed TMD and those who were healthy (mean difference 7.8 kg, 95% CI 1.4 to 14.2; P .01). Participants with mixed TMD were similar to those with myogenous
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Cervical Flexor Activity and Temporomandibular Disorders TMD in most of the general characteristics such as duration of complaint and pain intensity (P .05). Both groups had a moderate intensity of pain in the jaw and a long history of pain. Both groups also had a mild level of disability in the neck and a moderate level of disability in the jaw (Tab. 1). The Limitations of Daily Functions in TMD Questionnaire/Jaw Function Scale (JFS) disability score was signicantly higher for participants with mixed TMD compared with those with myogenous TMD (mean difference 4.1 points, 95% CI 1.4 to 6.9; P .001). The prevalence of neck pain in the sample of participants with TMD was high. Approximately 88% (87.5%) of the participants with myogenous TMD and 87.8% of those with mixed TMD had self-reported neck pain. Clinical Examination The participants underwent a clinical examination by a physical therapist with experience in musculoskeletal rehabilitation to determine eligibility for this study and to determine their diagnosis. The clinical examination followed the guidelines of the RDC/TMD.45 All participants read an informational letter and signed an informed consent statement in accordance with the University of Albertas policies on research using human subjects. Procedure Demographic data were collected on all participants who satised the inclusion criteria. In addition, all included participants were asked to report specic characteristics regarding their jaw problem (eg, onset, duration of symptoms, treatments received) and their intensity of pain in the jaw (VAS score)49,5558 and to complete the Neck Disability Index (NDI),59,60 the JFS,61 and a questionnaire for history of jaw pain used by the RDC/TMD.45 In addition, participants were asked to complete
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the Chronic Pain Grade Disability Questionnaire for TMD used by the RDC/TMD to evaluate the level of chronic disability due to TMDs.45 The reliability and validity of these tools have been reported elsewhere.45,59 61 After the participants were evaluated clinically and had completed the questionnaires, they performed the CCFT. This testing was performed in one session. Electromyographic Evaluation of the Cervical Flexor Muscles Electrode placement. Surface electrodes were located on the sternal head of the SCM muscle and on the AS muscle as described in the protocol used by Falla and colleagues.62,63 A reference electrode was placed on the wrist. Normalization procedure for EMG data. For normalization purposes, EMG data were collected for 5 seconds during a maximal voluntary contraction (MVC). The EMG activity of the SCM and AS muscles was recorded during this maximal contraction and saved in the computer. This procedure was repeated a second time. Submaximal contractions obtained during the CCFT were normalized using these 2 MVC values. Submaximal contractions were expressed as a percentage of the 3-second root mean square (RMS) value obtained during the MVC. The average between the normalized contractions using the 2 MVC measurements was used for statistical analysis. EMG data processing. Data on EMG activity of the SCM and AS muscles were obtained using the Bagnoli-8 EMG system* in a bipolar conguration with DE-2.1 electrodes.* This system is designed to make the acquisition of EMG signals easy and reliable (common-mode rejection ratio 92 dB, system
* Delsys Inc, PO Box 15734, Boston, MA 02215.

noise 1.2 V [RMS]). The EMG activity was recorded (analog raw signal) with a data acquisition program, written in Labview 7.1, which collected data at 1,024 Hz using a PCMCIA card ltered between 20 and 450/Hz 10% and amplied using a gain of 1,000 according to the established standards for EMG acquisition and reporting.64,65 To obtain a measure of EMG amplitude, maximum root mean square (RMS) was calculated for 4 seconds during the 10-second submaximal contractions for each muscle while performing the CCFT using IGOR Pro5.1 and was expressed a percentage of the 3-second EMG activity obtained during the MVC normalization procedure. Instrumentation for Registering the Pressure Exerted While Performing the CCFT An air-lled pressure sensor (pressure biofeedback unit) was placed in the suboccipital region of each patients neck and inated to a pressure of 20 mm Hg. The cuff was connected to a pressure transducer (miniature pressure cell) designed to register increases in pressure with the movement of nodding action for the CCFT. Electrical signals from the pressure transducer were amplied to a visual feedback device and projected onto a computer screen so that the participants were able to see the targeted pressure level. Graphs with the performance of each participant during the CCFT were stored using Igor Pro5.1. These data were analyzed ofine by a blinded assessor. Craniocervical Flexion Test: Description and Procedures Before testing began, participants were asked to perform a warm-up, which consisted of 2 movements of the neck and head in all directions
National Instruments Corporation, 11500 N Mopac Expwy, Austin, TX 78759-3504. WaveMetrics Inc, PO Box 2088, Lake Oswego, OR 97035.

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Cervical Flexor Activity and Temporomandibular Disorders (exion [forward neck movement], extension, side exion [lateral movement of the neck], and rotation). The participants were placed in a relaxed supine position with the knees exed and the head and neck maintained in a mid-position (ie, neutral position, no exion or extension) following a protocol established previously.66 The head and chin were parallel to the plinth (Fig. 1). The CCFT is a low-load test that is the most common method used to evaluate the performance of the deep cervical muscles (ie, longus colli and rectus capitis). The CCFT consists of a craniocervical exion (nodding) movement, which combines the action of exion at the craniocervical junction, performed by the longus capitis muscles, along with the attening of the cervical lordosis, an action of the longus colli muscles. Electromyographic activity of the supercial cervical exor muscles such as the SCM and AS may be registered during the CCFT. Elevated EMG activity may be a compensation for reduced or impaired activity of the deep cervical exor muscles in individuals with cervical-associated pain compared with those who are healthy.67 The CCFT required each participant to perform the craniocervical exion movement in 5 progressive stages of increasing pressure (22, 24, 26, 28, and 30 mm Hg) with the aid of a visual feedback device. Participants were instructed to perform this gentle nodding movement (craniocervical exion) and at practiced progressive targeted pressure levels. The order of the targeted pressure level was randomized by an independent assessor. Participants had to maintain a steady pressure at each targeted level for a duration of 10 seconds (Fig. 1). They repeated each targeted level 2 times, with a rest period of 1 minute between repetitions to avoid the effects of fatigue.68
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Figure 1.
Craniocervical exion test.

Data Analysis The normalized data of the EMG activity of all muscles were analyzed descriptively (ie, mean, standard deviation). Variables were tested for normality, homogeneity of variance, and linearity. All EMG variables were reasonably normally distributed. Histograms and box plots show that most of the variables were slightly skewed to the right. However, ANOVA analysis is robust to these mild deviations from normality and can provide accurate estimates of the analyzed variables.69 A 3-way mixed-design ANOVA for repeated measures (3 independent variables: muscles [SCM and AS], test [5 levels], and groups [myogenous TMD, mixed TMD, and control]) was used to evaluate the differences in EMG activity for selected muscles (dependent variable) while performing the CCFT at 5 levels of pressure.

Pair-wise comparisons using the Bonferroni procedure were administered to evaluate the differences between variables and groups (ie, control and TMD groups) in all of the different conditions (objective 1). The Spearman rho test was used to evaluate the relationship among NDI, JFS, and clinical variables with EMG variables (correlational matrix) (objectives 2 and 3). The correlation was considered important when the correlation coefcient value was higher than .70. The reference values to make this decision were based on values reported by Munro.70 To clearly show the impact of the results for clinical practice, clinical relevance of the results was assessed using a distribution-based method.71 The effect size (Cohen d) values were calculated to determine clinical relevance of the differences in the EMG measurements across different
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Cervical Flexor Activity and Temporomandibular Disorders

Myogenous TMD
60 Normalized EMG Activity (%MVC) 50 40 30 20 10 0

Healthy

Mixed TMD

Figure 2.
Normalized electromyographic (EMG) activity of sternocleidomastoid (SCM) and anterior scalene (AS) muscles in participants with myogenous temporomandibular disorders (TMD), those with mixed TMD, and those who were healthy while performing the craniocervical exion test. Error bars 95% condence interval. %MVC percentage of maximum voluntary contraction, AvSCMR_22mmHg average right SCM muscle EMG activity at 22 mm Hg, AvSCML_22mmHg average left SCM muscle EMG activity at 22 mm Hg, AvASR_22mmHG average right AS muscle EMG activity at 22 mm Hg, AvASL_22mmHg average left AS muscle EMG activity at 22 mm Hg, AvSCMR_24mmHg average right SCM muscle EMG activity at 24 mm Hg, AvSCML_24mmHg average left SCM muscle EMG activity at 24 mm Hg, AvASR_24mmHg average right AS muscle EMG activity at 24 mm Hg, AvASL_24mmHg average left AS muscle EMG activity at 24 mm Hg, AvSCMR_26mmHg average right SCM muscle EMG activity at 26 mm Hg, AvSCML_26mmHg average left SCM muscle EMG activity at 26 mm Hg, AvASR_26mmHg average right AS muscle EMG activity at 26 mm Hg, AvASL_26mmHg average left AS muscle EMG activity at 26 mm Hg, AvSCMR_28mmHg average right SCM muscle EMG activity at 28 mm Hg, AvSCML_28mmHg average left SCM muscle EMG activity at 28 mm Hg, AvASR_28mmHg average right AS muscle EMG activity at 28 mm Hg, AvASL_28mmHg average left AS muscle EMG activity at 28 mm Hg, AvSCMR_30mmHg average right SCM muscle EMG activity at 30 mm Hg, AvSCML_30mmHg average left SCM muscle EMG activity at 30 mm Hg, AvASR_30mmHg average right AS muscle EMG activity at 30 mm Hg, AvASL_30mmHg average left AS muscle EMG activity at 30 mm Hg.

levels of pressure and groups.72 Effect sizes of 0.4 or higher were considered clinically relevant.73 A subgroup analysis also was conducted to determine differences between participants with pure TMD (ie, without neck pain) and those who were healthy. The level of signicance was set at .05. The SPSS version 17 and STATA version 10 statistical programs were used to perform the statistical analysis. The analysis was performed blinded to group condition.

SPSS Inc, 233 S Wacker Dr, Chicago, IL 60606. StataCorp LP, 4905 Lakeway Dr, College Station, TX 77845.

AvASL_30mmHg AvASR_30mmHg AvSCML_30mmHg AvSCMR_30mmHg AvASL_28mmHg AvASR_28mmHg AvSCML_28mmHg AvSCMR_28mmHg AvASL_26mmHg AvASR_26mmHg AvSCML_26mmHg AvSCMR_26mmHg AvASL_24mmHg AvASR_24mmHg AvSCML_24mmHg AvSCMR_24mmHg AvASL_22mmHg AvASR_22mmHg AvSCML_22mmHg AvSCMR_22mmHg

AvASL_30mmHg AvASR_30mmHg AvSCML_30mmHg AvSCMR_30mmHg AvASL_28mmHg AvASR_28mmHg AvSCML_28mmHg AvSCMR_28mmHg AvASL_26mmHg AvASR_26mmHg AvSCML_26mmHg AvSCMR_26mmHg AvASL_24mmHg AvASR_24mmHg AvSCML_24mmHg AvSCMR_24mmHg AvASL_22mmHg AvASR_22mmHg AvSCML_22mmHg AvSCMR_22mmHg

Results
EMG Activity of the Cervical Flexors Muscles While Performing the CCFT Large variability of the normalized EMG activity across conditions and groups was observed (Fig. 2). Using a 3-way mixed-design ANOVA for repeated measures, we found that the main effects of muscles (F 18.5, P .0001) and pressure levels (F 27.3, P .0001) were statistically signicant. This nding means that there was a statistically signicant difference in EMG activity among muscles and among pressure levels. The interaction between muscles and pressure also was statistically signicant (F 2.9, P .001).

AvASL_30mmHg AvASR_30mmHg AvSCML_30mmHg AvSCMR_30mmHg AvASL_28mmHg AvASR_28mmHg AvSCML_28mmHg AvSCMR_28mmHg AvASL_26mmHg AvASR_26mmHg AvSCML_26mmHg AvSCMR_26mmHg AvASL_24mmHg AvASR_24mmHg AvSCML_24mmHg AvSCMR_24mmHg AvASL_22mmHg AvASR_22mmHg AvSCML_22mmHg AvSCMR_22mmHg

However, there was no signicant difference in EMG activity of the analyzed muscles among groups (ie, mixed TMD, myogenous TMD, and control) across conditions (F 2.6, P .07). Weight was not signicantly associated with EMG activity (P .49), so it was not included in the model. Subgroup Analysis: EMG Activity in Patients With Pure TMD (Without Neck Pain) Compared With Participants Who Were Healthy When analyzing a subgroup of participants with TMD but without neck pain (n 13) compared with the control group (n 47), statistically signicant differences in EMG
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Cervical Flexor Activity and Temporomandibular Disorders Table 2.

Subgroup Analysis Between Participants With Pure Temporomandibular Disorders and Participants Who Were Healthy: Electromyographic Activity of the Analyzed Muscles While Performing the Craniocervical Flexion Testa
95% Condence Interval for Difference Standard Error 3.315 3.719 4.580 5.149 2.715 3.380 2.922 3.637 4.393 3.981 6.631 Pb .017 .013 .035 .050 .045 .019 .045 .003 .050 .050 .033 Lower Bound 1.35 1.90 0.637 0.051 13.48 17.87 14.52 21.59 21.50 0.062 33.759 Upper Bound 17.68 20.22 23.20 24.86 0.11 1.22 0.124 3.68 0.014 19.55 1.093

Muscle SCMR

Pressure (mm Hg) 22 24 28 30

Group Myogenous TMD Myogenous TMD Myogenous TMD Myogenous TMD Healthy

Group Healthy Healthy Healthy Healthy Myogenous TMD Mixed TMD

Mean Difference Between Groups (%MVC) 9.51c 11.06c 11.92

c

12.17c 6.80
c

SCML

22

9.54c 7.32
c

24

Healthy

Myogenous TMD Mixed TMD

12.64c 10.68 9.74 17.43c

26 ASR ASL
a

Healthy Myogenous TMD Healthy

Mixed TMD Healthy Mixed TMD

22 24

Values based on estimated marginal means. TMD temporomandibular disorders, SCMR right sternocleidomastoid, SCML left sternocleidomastoid, ASR right anterior scalene, and ASL left anterior scalene. b Bonferroni adjustment for multiple comparisons. c The mean difference is signicant at the .05 level.

activity were found between groups (F 4.831, P .01). Post hoc analysis using a Bonferroni test indicated there were many statistically signicant differences between groups in the analyzed muscles and conditions (Tab. 2).

Association Between EMG Variables and Clinical Variables While Performing the CCFT Very weak (although statistically signicant) correlations were found, mainly between the EMG activity of the SCM muscles during the 5 stages

of the CCFT and clinical variables such as pain intensity, duration of complaint, neck disability, jaw disability, and level of chronic disability of TMD based on the RDC/TMD (Chronic Pain Grade Disability Questionnaire for TMDs) (Tab. 3).

Table 3.
Correlations Between Electromyographic Activity and Neck Disability (as Measured by Neck Disability Index), Chronic Pain Grade Classication, Jaw Disability (as Measured by Jaw Function Scale), Pain Intensity, and Duration of Complainta
Electromyographic Activity Average SCM at 22 mm Hg Average AS at 22 mm Hg Average SCM at 24 mm Hg Average AS at 24 mm Hg Average SCM at 26 mm Hg Average AS at 26 mm Hg Average SCM at 28 mm Hg Average AS at 28 mm Hg Average SCM at 30 mm Hg Average AS at 30 mm Hg
a

Neck Disability .23b .13 .23b .14 .18 .13 .18c .13 .24b .20c
c

Chronic Pain Grade Classication .26b .15 .26b .16 .19 .12 .17 .10 .21c .18c
c

Jaw Disability .26b .15 .30b .17c .24 .15 .23b .17
c b

Pain Intensity .32b .21

b

Duration of Complaint (y) .15 .05 .19c .08 .09 .04 .13 .03 .16c .11

.32b .21c .29b .21

b

.27b .22
b

.28b .22b

.33b .28b

SCM sternocleidomastoid muscle, AS anterior scalene muscle. b Correlation is signicant at the .05 level. c Correlation is signicant at the .01 level.

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Cervical Flexor Activity and Temporomandibular Disorders Table 4.

Moderate Effect Sizes for Comparisons Among Groups at Different Levels of Pressure While Performing the Craniocervical Flexion Testa
Raw Differences Condence Interval for Difference Outcome Measure: Electromyographic Activity Average SCMR at 22 mm Hg, mixed TMD vs healthy Average SCMR at 24 mm Hg, mixed TMD vs healthy Average SCMR at 28 mm Hg, mixed TMD vs healthy Average SCMR at 30 mm Hg, mixed TMD vs healthy Average SCML at 22 mm Hg, myogenous TMD vs healthy Average SCML at 22 mm Hg, mixed TMD vs healthy Average SCML at 24 mm Hg, myogenous TMD vs healthy Average SCML at 24 mm Hg, mixed TMD vs healthy Average SCML at 26 mm Hg, mixed TMD vs healthy Average SCML at 30 mm Hg, mixed TMD vs healthy Average ASR at 22 mm Hg, myogenous TMD vs healthy Average ASR at 30 mm Hg, myogenous TMD vs healthy Average ASR at 30 mm Hg, mixed TMD vs healthy Mean Difference (%MVC) 5.36 5.88 5.94 6.31 5.10 5.79 4.87 6.53 4.63 5.19 6.39 12.07 8.24 Lower Bound 1.65 1.83 0.77 0.67 0.66 2.06 0.79 2.49 0.25 0.06 0.49 1.02 0.17 Upper Bound 9.07 9.93 11.11 11.95 9.54 9.52 8.95 10.57 9.01 10.32 12.29 23.12 16.31 Effect Size 0.59 0.59 0.47 0.45 0.45 0.63 0.47 0.66 0.43 0.41 0.43 0.43 0.41 Standardized Effect Size Condence Interval for Effect Size Lower Bound 0.17 0.18 0.06 0.04 0.06 0.21 0.07 0.24 0.02 0.00 0.03 0.03 0.01 Upper Bound 0.99 0.99 0.87 0.85 0.85 1.03 0.87 1.06 0.83 0.81 0.82 0.82 0.81 Effect Size Based on Healthy Group Standard Deviation 0.73 0.72 0.54 0.48 0.72 0.82 0.66 0.89 0.50 0.42 0.60 0.72 0.49

a TMD temporomandibular disorders, SCMR right sternocleidomastoid muscle, SCML left sternocleidomastoid muscle, ASR right anterior scalene muscle, %MVC percentage of maximum voluntary contraction.

Clinical Relevance Effect sizes of comparisons between mixed TMD and myogenous TMD groups compared with the control group while performing the CCFT are displayed in Table 4 and Figures 3 and 4.

Discussion
The main nding of this study was that, although statistically signicant differences in EMG activity of the SCM and AS muscles in patients with TMD compared with participants who were healthy while performing the CCFT were not attained (P .07), there was a trend for patients with
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TMD to have consistently higher EMG activity in all of the analyzed muscles. This increased activity of the supercial muscles of the cervical spine might be associated with the neck disturbances seen in patients with TMD. This information may give clinicians insight into the importance of evaluation and possible treatment of the deep neck exors in patients with TMD. However, at this point, more research on these issues is necessary to provide denite conclusions. The results of this study cannot be directly compared with those of

other studies of cervical exor muscle performance in patients with TMD because no studies investigating this issue in this population were found. However, the CCFT has widely been used by physical therapists to determine alterations in the motor control of the craniocervical exor muscles in people with cervical disorders such as neck pain, whiplash-associated disorders, and cervicogenic headache because impairment of the deep exor muscles appears to be generic to neck disorders.37 All of the studies analyzing craniocervical performance using the CCFT36,63,74,75 converge in that
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Study or Subgroup ASR at 30 mm Hg SCML at 22 mm Hg SCML at 24 mm Hg SCML at 26 mm Hg SCML at 28 mm Hg SCML at 30 mm Hg SCMR at 22 mm Hg SCMR at 24 mm Hg SCMR at 28 mm Hg SCMR at 30 mm Hg Total (95% CI) Mixed TMD X 38.09 22.83 24.85 26.61 28.82 30.49 21.01 23.19 28.57 30.58 SD 22.55 10.83 11.93 12.07 12.5 12.93 10.59 11.48 14.25 14.5 Total 49 49 49 49 49 49 49 49 49 49 490 X 29.85 17.04 18.32 21.98 24.2 25.3 15.65 17.31 22.63 24.2 Healthy SD 16.7 7.09 7.36 9.29 10.4 12.35 7.34 8.15 10.98 13.27 Total 47 47 47 47 47 47 47 47 47 47 470 Weight 3.2% 14.8% 12.7% 10.7% 9.4% 7.7% 15.0% 12.5% 7.7% 6.4% 100.0% Mean Difference IV, Fixed, 95% CI 8.24 (0.32, 16.16) 5.79 (2.14, 9.44) 6.53 (2.58, 10.48) 4.63 (0.33, 8.93) 4.62 (0.03, 9.21) 5.19 (0.13, 10.25) 5.36 (1.73, 8.99) 5.88 (1.91, 9.85) 5.94 (0.86, 11.02) 6.38 (0.82, 11.94) 5.68 (4.27, 7.08) Mean Difference IV, Fixed, 95% CI

Heterogeneity: 2 1.16, df 9 (P 1.00), I2 0% Test for overall effect: Z 7.92 (P .00001)

Figure 3.
Moderate effect sizes found for comparisons between participants with mixed temporomandibular disorders (TMD) and those who were healthy at different levels of pressure while performing the craniocervical exion test. IV inverse variance, 95% CI 95% condence interval, ASR right anterior scalene muscle, SCML left sternocleidomastoid muscle, SCMR right sternocleidomastoid muscle.

patients with cervical involvement have an impaired performance of the deep and supercial exor cervical muscles. The increased activity in the supercial muscles could be seen as a strategy to compensate for the dysfunction of the deep exor muscles. Sterling et al76 suggested that the presence of pain could lead to inhibition or delayed activation of

specic muscles or group of muscles in the spine. This inhibition generally occurs in deep muscles such as the longus colli and longus capitis, which control joint stability.76 The results of this study are not in total agreement with those of the majority of the above-mentioned studies. In our study, we found no

statistically signicant differences in supercial cervical exor muscular activity among groups while performing the CCFT, as evaluated though EMG analysis. One possible explanation for these results could be the level of dysfunction presented by the participants with TMD. We found that the level of dysfunction, not only at the level of the neck but

Study or Subgroup ASR at 22 mm Hg ASR at 30 mm Hg SCML at 22 mm Hg SCML at 24 mm Hg Total (95% CI)

Myogenous TMD X 26.05 41.92 22.14 23.19 SD 17.83 34.82 13.83 12.3 Total 54 54 54 54 216 X 19.66 29.85 17.04 18.32

Healthy SD 10.59 16.73 7.09 7.36 Total 47 47 47 47 188 Weight 19.3% 5.6% 34.7% 40.4% 100.0%

Mean Difference IV, Fixed, 95% CI 6.39 (0.75, 12.03) 12.07 (1.62, 22.52) 5.10 (0.89, 9.31) 4.87 (0.97, 8.77) 5.65 (3.17, 8.13)

Mean Difference IV, Fixed, 95% CI

Heterogeneity: 2 1.74, df 3 (P .63), I2 0% Test for overall effect: Z 4.47 (P .00001)

Figure 4.
Moderate effect sizes found for comparisons between participants with myogenous temporomandibular disorders (TMD) and those who were healthy at different levels of pressure while performing the craniocervical exion test. IV inverse variance, 95% CI 95% condence interval, ASR right anterior scalene muscle, SCML left sternocleidomastoid muscle.

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Cervical Flexor Activity and Temporomandibular Disorders also at the level of the jaw, was considered mild for our participants with TMD. We might speculate that because the disability was mild, it did not have an impact on function or physical impairment, which generally is found in people with more disabling pain. Our results are in agreement with the results obtained by Falla et al63 in individuals with a level of disability similar to that of the participants in this present study (mean NDI score 12.4 points, SD 9.563). Falla et al63 found that even though the normalized EMG amplitude of the deep cervical exor muscles was signicantly lower in patients with neck pain compared with individuals who were healthy (P .05), the increase in EMG activity of the supercial muscles did not reach statistical signicance, although there was a trend of increased EMG activity for the supercial muscles in patients with neck pain. The main explanation of this nding was the large variability in the EMG activity found across groups and conditions. These results agree with our ndings, which also showed a large amount of variability in EMG activity among muscles and conditions (as evidenced by the wide CIs). When interpreting CIs, lower and upper boundaries need to be taken into account to make conclusions.77 Based on this interpretation, we can say that 95% of the time the estimated difference between groups could fall between these lower and upper boundaries. If we look at the upper boundaries of the CIs for the raw mean differences (Tab. 4), we can see that the difference between groups can be as high as 8.95% to 23.12% of MVC. However, if we look at the lower boundaries, the difference between groups can be as low as 0.06% to 2.49% of MVC. Therefore, based on this large variability, we could have a situation where a clinically signicant difference between groups as well as a nonclinically signicant difference between groups could occur. Although there was great variability in EMG activity, the mean EMG activity of the supercial muscles was always higher for participants with TMD pain compared with the control group across all conditions and muscles (Fig. 2). However, the large variability of the normalized EMG activity across participants and groups did not lead to a nding of statistical signicance. The large variability seen in the EMG activity of the cervical exor muscles also has been observed in other regions such as the low back.78 Hodges et al78 found that people responded differently to experimental pain in the low back muscles. They reported that no 2 individuals showed identical patterns of increased activity of the low back muscles when they underwent experimental pain. If this phenomenon were extrapolated to the cervical spine, it could be speculated that each individual has a different muscle activation strategy to adapt to pain. The motor response in the cervical spine, especially in people with pain, would be an increase of the activity of the SCM and AS muscles; however other strategies, using different muscles not investigated in this research, also could be present. Further research investigating possible cervical motor strategies in people with TMD under different conditions would help further clarify the role of the cervical muscles in TMD. Our study did not measure directly the activity of the deep cervical exor muscles because the technique for measuring the activity of the deep cervical muscles is invasive and adherence to the testing protocol would have been impaired. We measured the supercial cervical muscles such as the SCM and AS only as an indirect measure of impairment of the activity of the deep cervical exor muscles. Thus, it is still uncertain whether deep cervical muscle activity was impaired in these patients. In addition, because the cervical spine is a very complex system characterized by a high degree of redundancy in the muscular system,36,79 it is not surprising that other motor strategies and muscles not analyzed in this study (other than SCM and AS muscles) could be used by people with pain to stabilize the cervical spine. The CCFT has become a gold standard for isolating the activation of the deep exor muscles and identifying possible co-contraction patterns of supercial muscles in the cervical spine.63,75,80 Its construct validity66,81 as well as its reliability67 have been established; however, other psychometric properties such as concurrent validity with clinical variables such as neck disability and pain intensity of this test need to be ascertained. Thus, this study investigated the associations between the muscular activity of the analyzed muscles through the 5 stages of the CCFT and clinical variables such as the level of chronic pain grade classication of TMD based on the RDC/TMD, pain intensity, time of complaint, jaw disability, and neck disability. Most of the associations were positive but weak, indicating that the performance of the CCFT is not strongly related to other clinical variables such as pain intensity, neck disability, or jaw disability. These results are in agreement with those of Falla et al,82 who reported that reduction in pain in patients with neck pain after a training program was not accompanied by an improvement in performance of the cervical exor muscles. It appears that pain and physical performance of the craniocervical muscles represent different aspects of disability in people with cervical involvement.83 Thus, a more focused evaluation
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Cervical Flexor Activity and Temporomandibular Disorders regarding disability and its related factors in future research is needed to understand the intricacies among physical impairments, pain, and disability. Because of the variability of EMG activity among groups and conditions found in this study, an analysis of the clinical relevance of the results through the calculation of effect sizes was conducted to evaluate the relevance of these ndings. To our knowledge, this is the rst time that a study has evaluated the clinical relevance of EMG activity. According to Musselman,71 effect size calculation is one of the most common ways to evaluate clinical relevance after the fact.71,84 The larger this effect size index, the larger the difference between groups and the larger the clinical relevance of the results.71 It is recognized that effect sizes of 0.2, 0.5, and 0.8 correspond to small, moderate, and large effects.73 Although there is no known research that establishes a cutoff of EMG activity (percentage of MVC) to be considered clinically relevant when comparing the EMG activity of different groups, it has been shown that EMG activity as low as 2% to 5% of MVC can be related to pain in neck-shoulder areas.85 87 In addition, a minimally important difference for EMG activity has been found to be 2.9% of MVC.88 Although a large variability in the estimates of effect sizes was present in this data set (which had wide CIs), based on the calculated mean effect sizes (ie, standardized mean differences ranging between 0.41 and 0.66) and the raw mean differences obtained from the comparisons (ranging from 4.63% to 12.07% of MVC), differences in EMG activity were found in some of the comparisons between patients with TMD and the control group (Tab. 3). Thus, standardized effect sizes and minimally important difference could
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serve as an index to guide clinicians in the relevance of the ndings. It could be said that in the absence of knowledge and guidelines to determine the clinical relevance of certain outcomes, calculation of the clinical relevance, based on the distribution methods, could be an option. These results could be of importance for clinicians who work in this eld because this analysis might indicate that patients with TMD tended to have increased activity of the supercial cervical muscles compared with the control group. In addition, the results of the subgroup analysis considering only patients with pure TMD provide more support for these ndings. Furthermore, preliminary evidence has shown that exercises addressing these types of impairments (ie, training of neck exor muscles) as part of cervical spine treatment in people with TMD reduced pain and improved function (ie, increased pain-free mouth opening) in patients with TMD, which potentially supports the fact that patients with TMD could benet from treatment of impaired cervical exor muscles.89 Therefore, these results might be considered when evaluating and treating patients with TMD. Nevertheless, it is necessary to implement a randomized controlled trial that addresses these cervical impairments through cervical exor exercises in patients with TMD and test whether these exercises decrease pain and improve function and quality of life in patients with TMD. In this way, research could advance clinical practice in this area. Limitations The results obtained in this research are applicable for the group of individuals who participated in this study under the protocols used. They potentially could be applied to people with TMD having characteristics similar to those of the partici-

pants in this study. This limitation should be taking into consideration when attempting to extrapolate these results. In addition, it must be acknowledged that because this project was cross-sectional, a causeand-effect relationship between cervical muscular impairment and TMD cannot be established.

Conclusions
There were no statistically signicant differences (P .07) in EMG activity in the SCM or the AS muscles in patients with mixed and myogenous TMD compared with individuals who were healthy when performing the CCFT. However, the patients with TMD tended to have increased activity of the supercial cervical muscles compared with the control group. This increased activity of the supercial muscles of the cervical spine might be associated with the neck disturbances seen in patients with TMD. This information may give clinicians insight into the importance of evaluation and possible treatment of the deep neck exors in patients with TMD. However, future research should test the effectiveness of this type of program through a randomized controlled trial in individuals with TMD to determine the real value of treating this type of impairment in this population.
Dr Armijo-Olivo, Dr Warren, Dr Major, and Dr Magee provided concept/idea/research design. Dr Armijo-Olivo, Mr da Costa, Dr Gadotti, Dr Major, Dr Thie, and Dr Magee provided writing. Dr Armijo-Olivo, Mr Fuentes, Mr da Costa, and Dr Gadotti provided data collection. Dr Armijo-Olivo and Dr Warren provided data analysis. Dr Armijo-Olivo and Dr Magee provided project management. Dr Armijo-Olivo provided fund procurement. Dr Magee provided facilities/ equipment and institutional liaisons. Dr Armijo-Olivo, Mr Fuentes, Mr da Costa, Dr Gadotti, Dr Warren, Dr Major, Dr Thie, and Dr Magee provided consultation (including review of manuscript before submission). The authors thank all of the participants in this study and Darrel Goertzen, Luis Cam-

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pos, and Rodrigo Guzman for their technical assistance. The study was approved by the Ethics Committee of the University of Alberta, Edmonton, Alberta, Canada. This research was presented at the XVIII International Conference of the International Society of Electrophysiology and Kinesiology, June 16 19, 2010, Aalborg, Denmark; the 5th International Conference on Orofacial Pain and Temporomandibular Disorders, August 26 30, 2009, Praia do Forte, Bahia, Brazil; and the 13th World Conference on Pain, August 29 September 2, 2010, Montreal, Quebec, Canada. Dr Armijo-Olivo was supported by the Canadian Institutes of Health Research (CIHR), the Alberta Provincial CIHR Training Program in Bone and Joint Health, an Izaak Walton Killam Scholarship from the University of Alberta, and the Physiotherapy Foundation of Canada through an Ann Collins Whitmore Memorial Award. Mr Fuentes is supported by the government of Chile (BECAS Chile Scholarship Program) and Catholic University of Maule, Chile. 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Electromyographic Activity of the Cervical Flexor Muscles in Patients With Temporomandibular Disorders While Performing the Craniocervical Flexion Test: A Cross-Sectional Study Susan Armijo-Olivo, Rony Silvestre, Jorge Fuentes, Bruno R. da Costa, Inae C. Gadotti, Sharon Warren, Paul W. Major, Norman M.R. Thie and David J. Magee PHYS THER. 2011; 91:1184-1197. Originally published online June 9, 2011 doi: 10.2522/ptj.20100233 References This article cites 73 articles, 7 of which you can access for free at: http://ptjournal.apta.org/content/91/8/1184#BIBL http://ptjournal.apta.org/subscriptions/

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