Original Research Cervical Muscle Area Measurements in Acute Whiplash Patients and Controls Erika J. Ulbrich, MD, 1,2 * Suzanne E. Anderson, MD, 2,3 Andre Busato, PhD, 4 Susanne Abderhalden, MD, 2,5 Chris Boesch, MD, PhD, 6 Heinz Zimmermann, MD, 7 Paul Heini, MD, 8 Juerg Hodler, MD, PhD, 5 and Matthias Sturzenegger, MD 9 Purpose: To quantitatively compare the muscle cross-sec- tional areas (CSAs) of the cervical muscles in sympto- matic acute whiplash patients versus healthy controls. We hypothesized, that symptomatic whiplash patients have smaller cervical muscle CSAs than matched controls and that smaller cervical muscle CSAs in women might explain that women more frequently are symptomatic af- ter whiplash injury than men. Materials and Methods: Prospective controlled study. Thirty-eight consecutive acute whiplash patients were examined within 48 h after a motor vehicle accident and 38 healthy age- and sex-matched controls, each half female, half male, were examined with the same protocol. MRI CSA measurements were performed of the deep and total cervical extensor muscles as well as the sternoclei- domastoid muscles using transversal STIR (Short T1 Inversion Recovery) sequences on level C2, C4, and C5 by two blinded raters. Clinical symptoms were assessed with patient questionnaires (EuroQuol 5D, Specific Whiplash Questionnaire, head- and neck pain intensity [VAS]). Results: Agreement of measurements between the two raters was high (intraclass correlation 0.52 to 0.85 for the different levels). No significant difference in age and body mass index were seen between patients and controls and the distribution of genders across groups was identical. There were no significant differences between patients and controls for all CSAs. Women had consistently smaller CSAs than men. The CSAs showed no significant correlation with the pain intensity of neck pain and head- ache but a consistent tendency of less neck pain and more headache with greater CSAs. Conclusion: This small study provides no evidence that subjects with smaller CSAs of cervical extensor muscles have a higher risk in developing symptoms after a whip- lash injury and confirms smaller CSA in women. Key Words: MRI; cross-sectional areas (CSAs); cervical extensor muscles; MRI muscle; symptomatic acute whip- lash patients J. Magn. Reson. Imaging 2011;33:668–675. V C 2011 Wiley-Liss, Inc. NECK AND HEAD pain are the most prominent symp- toms in the acute and chronic phase after whiplash injury. The responsible tissue damage is disputed, and no consistent findings regarding for example muscle edema or hemorrhage or ligamentous tears have been confirmed (1). Factors determining whether a patient becomes symptomatic after a whiplash injury or not as reported in the literature range from the structural to psychological (2–4). As there was lit- tle available information about the effect of cervical muscle volumes on acute whiplash-associated injury, our study was designed to review this. We took a novel approach by aiming at reviewing patients within a 48-h period from the motor vehicle accident (MVA) and using as special MR imaging protocol. Findings suggesting that cervical muscles play a role in whiplash-associated disorders (WAD) are as follows: Patients aware of an impending impact and/ or with precontracted neck muscles have less acute and chronic symptoms (5); Women are more fre- quently symptomatic than men (6,7); and Chronic 1 Department of Radiology, Orthopedic University Hospital Balgrist, Zu ¨ rich, Switzerland. 2 Department of Diagnostic, Interventional and Pediatric Radiology, Inselspital, Bern University Hospital, and University of Bern, Switzerland. 3 School of Medicine, Medical Imaging, The University of Notre Dame Sydney, Darlinghurst Campus, Australia. 4 Institute for Evaluative Research in Orthopedic Surgery, University of Bern, Switzerland. 5 Department of Radiology, USZ, University Hospital Zu ¨ rich, Switzerland. 6 Department of Clinical Research, Magnetic Resonance Spectroscopy and Methodology, University of Bern, Switzerland. 7 Department of Emergency, Inselspital, Bern University Hospital, and University of Bern, Switzerland. 8 Department of Orthopedics, Inselspital, Bern University Hospital, and University of Bern, Switzerland. 9 Department of Neurology, Inselspital, Bern University Hospital, and University of Bern, Switzerland. This work was performed at Department of Diagnostic, Interventional and Pediatric Radiology, Inselspital, Bern University Hospital, and University of Bern, Bern, Switzerland. Contract grant sponsor: the Swiss National Science Foundation; Contract grant number: 405340-104531. *Address reprint requests to: E.J.U., Orthopedic University Hospital Balgrist, Forchstrasse 340, 8008 Zurich, Switzerland. E-mail: [email protected] Received August 4, 2010; Accepted October 20, 2010. DOI 10.1002/jmri.22446 View this article online at wileyonlinelibrary.com. JOURNAL OF MAGNETIC RESONANCE IMAGING 33:668–675 (2011) CME V C 2011 Wiley-Liss, Inc. 668 15222586, 2011, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jmri.22446 by Readcube (Labtiva Inc.), Wiley Online Library on [22/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
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Cervical muscle area measurements in acute whiplash patients and controlsCervical Muscle Area Measurements in Acute Whiplash Patients and Controls
Erika J. Ulbrich, MD,1,2* Suzanne E. Anderson, MD,2,3 Andre Busato, PhD,4
Susanne Abderhalden, MD,2,5 Chris Boesch, MD, PhD,6 Heinz Zimmermann, MD,7
Paul Heini, MD,8 Juerg Hodler, MD, PhD,5 and Matthias Sturzenegger, MD9
Purpose: To quantitatively compare the muscle cross-sec- tional areas (CSAs) of the cervical muscles in sympto- matic acute whiplash patients versus healthy controls. We hypothesized, that symptomatic whiplash patients have smaller cervical muscle CSAs than matched controls and that smaller cervical muscle CSAs in women might explain that women more frequently are symptomatic af- ter whiplash injury than men.
Materials and Methods: Prospective controlled study. Thirty-eight consecutive acute whiplash patients were examined within 48 h after a motor vehicle accident and 38 healthy age- and sex-matched controls, each half female, half male, were examined with the same protocol. MRI CSA measurements were performed of the deep and total cervical extensor muscles as well as the sternoclei- domastoid muscles using transversal STIR (Short T1 Inversion Recovery) sequences on level C2, C4, and C5 by two blinded raters. Clinical symptoms were assessed with
patient questionnaires (EuroQuol 5D, Specific Whiplash Questionnaire, head- and neck pain intensity [VAS]).
Results: Agreement of measurements between the two raters was high (intraclass correlation 0.52 to 0.85 for the different levels). No significant difference in age and body mass index were seen between patients and controls and the distribution of genders across groups was identical. There were no significant differences between patients and controls for all CSAs. Women had consistently smaller CSAs than men. The CSAs showed no significant correlation with the pain intensity of neck pain and head- ache but a consistent tendency of less neck pain and more headache with greater CSAs.
Conclusion: This small study provides no evidence that subjects with smaller CSAs of cervical extensor muscles have a higher risk in developing symptoms after a whip- lash injury and confirms smaller CSA in women.
Key Words: MRI; cross-sectional areas (CSAs); cervical extensor muscles; MRI muscle; symptomatic acute whip- lash patients J. Magn. Reson. Imaging 2011;33:668–675. VC 2011 Wiley-Liss, Inc.
NECK AND HEAD pain are the most prominent symp- toms in the acute and chronic phase after whiplash injury. The responsible tissue damage is disputed, and no consistent findings regarding for example muscle edema or hemorrhage or ligamentous tears have been confirmed (1). Factors determining whether a patient becomes symptomatic after a whiplash injury or not as reported in the literature range from the structural to psychological (2–4). As there was lit- tle available information about the effect of cervical muscle volumes on acute whiplash-associated injury, our study was designed to review this. We took a novel approach by aiming at reviewing patients within a 48-h period from the motor vehicle accident (MVA) and using as special MR imaging protocol.
Findings suggesting that cervical muscles play a role in whiplash-associated disorders (WAD) are as follows: Patients aware of an impending impact and/ or with precontracted neck muscles have less acute and chronic symptoms (5); Women are more fre- quently symptomatic than men (6,7); and Chronic
1Department of Radiology, Orthopedic University Hospital Balgrist, Zurich, Switzerland. 2Department of Diagnostic, Interventional and Pediatric Radiology, Inselspital, Bern University Hospital, and University of Bern, Switzerland. 3School of Medicine, Medical Imaging, The University of Notre Dame Sydney, Darlinghurst Campus, Australia. 4Institute for Evaluative Research in Orthopedic Surgery, University of Bern, Switzerland. 5Department of Radiology, USZ, University Hospital Zurich, Switzerland. 6Department of Clinical Research, Magnetic Resonance Spectroscopy and Methodology, University of Bern, Switzerland. 7Department of Emergency, Inselspital, Bern University Hospital, and University of Bern, Switzerland. 8Department of Orthopedics, Inselspital, Bern University Hospital, and University of Bern, Switzerland. 9Department of Neurology, Inselspital, Bern University Hospital, and University of Bern, Switzerland.
This work was performed at Department of Diagnostic, Interventional and Pediatric Radiology, Inselspital, Bern University Hospital, and University of Bern, Bern, Switzerland.
Contract grant sponsor: the Swiss National Science Foundation; Contract grant number: 405340-104531.
*Address reprint requests to: E.J.U., Orthopedic University Hospital Balgrist, Forchstrasse 340, 8008 Zurich, Switzerland. E-mail: [email protected]
Received August 4, 2010; Accepted October 20, 2010.
DOI 10.1002/jmri.22446 View this article online at wileyonlinelibrary.com.
JOURNAL OF MAGNETIC RESONANCE IMAGING 33:668–675 (2011)
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whiplash patients show smaller cervical spine muscle volumes and fatty infiltration compared with controls (8). However, the reduced muscle volumes in chronic whiplash patients may be a secondary phenomenon due to inactivity and these findings cannot be neces- sarily applied to investigate the role of cervical muscle volumes in the acute symptom genesis of whiplash patients.
Previous studies have reviewed whiplash patients af- ter varied time periods and documented altered mus- cle strength (9) or muscle endurance (10,11) as a con- sequence of neck pain, whether following a whiplash injury or not. Analyzing cervical range of motion does not discriminate between muscles and joints (12).
Quantitative paraspinal muscle volume assessment using cross-sectional area measurements have been performed in chronic whiplash patients and compared with healthy controls using ultrasound (13) and MRI (14,15) (females only).
This study allowed for measurements to be per- formed on muscles in consecutive acute whiplash patients (both genders) using MRI routinely within a 48-h period after MVA.
The objective of this study was to quantitatively compare the muscle cross-sectional areas (CSAs) as surrogate markers for muscle volumes of cervical ex- tensor muscles (deep and total dorsal cervical muscles at C2 and C5 level) and the sternocleidomas- toid muscles (at C4 level) at predefined multiple cervi- cal levels in symptomatic acute whiplash patients ver- sus healthy controls. Our first hypothesis was that symptomatic whiplash patients have smaller muscle areas compared with sex- and age-matched healthy asymptomatic controls as a predisposing factor. Our second hypothesis was that women are at an increased risk of being symptomatic compared with men after a whiplash injury due to smaller cervical muscle volumes.
MATERIALS AND METHODS
The responsible ethics committee and agency for au- thorization of therapeutic products approved this pro- spective study, and written informed consent was obtained from all patients and controls before study inclusion.
Subjects
Patients presenting with acute whiplash injury Grade I or II, as defined by Quebec task force (16) following a rear-end MVA with a mechanism of forceful flexion and extension of the cervical spine with persistent symptoms of at least neck pain and stiffness, were eli- gible for recruitment. A total of 76 subjects (38 con- secutive acute whiplash patients, 38 healthy controls, with half female, half male each) with an average age of 35.1 years (standard deviation [SD] 14.0 years) were recruited from the emergency department if the results for inclusion and exclusion criteria ascer- tained with standardized questionnaires where appro- priate and underwent MRI examination within 48 h
after injury. Inclusion criteria for acute whiplash patients and healthy controls included age older than 18 years and signed written informed consent. All patients were first clinically reviewed by emergency medical staff to exclude serious injury, such as unsta- ble multiple trauma, spinal fracture, and subluxation or dislocation that may necessitate immediate surgi- cal stabilization. Whiplash patients were excluded if they had a fracture or subluxation of the cervical spine as diagnosed on standard radiographs and/or computed tomography (CT), direct head injury, previ- ous surgery or neurosurgery to the head or spine, pre- vious history of whiplash with persisting pain, muscu- loskeletal inflammatory disorders or other severe illness (with continuous pain or reduction of working ability), pre-existing head and neck pain, psychiatric disorders, drug or alcohol abuse, tumor/metastases of the head and neck, claustrophobia, pacemaker, or pregnancy.
For controls, healthy asymptomatic volunteers were recruited by advertisement within the local university and were matched to patients for age and sex. The same eligibility criteria were used as for the patient group where applicable. Here, age- and sex-matched subjects having suffered a whiplash injury without consecutive symptoms would be the optimal control group, but these cases are extremely difficult to recruit for obvious reasons.
Clinical Symptoms
Symptoms in the patient group were assessed using patient questionnaires: EuroQuol 5D, Specific Whip- lash Questionnaire and visual analog scales (VAS) for head and neck pain intensity. The head and neck pain intensity scales were graded from 0 (no pain) to 100 (maximum of pain).
MRI Acquisition and Protocol
MR images were obtained using a SONATA 1.5 Tesla (T) magnet (Siemens Medical Solutions, Erlangen, Germany). All patients and healthy controls had the same MR protocol. Sagittal and transverse STIR/TIRM (Short Tau Inversion Recovery/Turbo Inversion Recov- ery Magnitude) sequences obtained as part of the larger study protocol were used for this substudy to review the muscles. The total scan time was 15 min 23 s. Parameters for the sagittal TIRM sequence con- sisted of repetition time (TR) 4860 ms, echo time (TE) 28 ms, inversion time 150 ms, flip angle 180, turbo factor 7, total acquisition time 5 min 47 s. Two trans- versal TIRM sequences with TR 5110 ms, TE 28 ms, inversion time 150 ms, flip angle 180, turbo factor 7, and total acquisition time 4 min 48 s each were com- bined to cover the region of interest. All images were acquired on a 512 256 pixel matrix with a 210 mm 158 mm field of view and a slice thickness of 3 mm. A dedicated neck coil and a spine array coil were used with the patient in the supine position. Saturation pulses placed over the upper airway region were used for fat/water suppression and to remove flow artifacts.
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Sagittal and transverse slices of the cervical spine were obtained from the midpoint of the cerebellum through to the second thoracic vertebral level to include the entire cervical extensor musculature. The 19 sagittal images were centered on the spinal cord at the C4 level. The 20 transverse images per slab were planned on the sagittal sequence and were performed with two overlapping slabs which were perpendicular to the posterior surface of the vertebral body in the middle of the respective slab. Three slabs were used, if required, to cover the entire region. The tilt of the transverse images was thus adapted to the vertebral body orientation. Each transverse slab included 20 images.
Imaging Analysis
Muscle CSA were taken as surrogate markers for muscle volumes (14,15), instead of doing muscle vol-
umes, to be in line with previous investigations to allow for review. Two blinded radiologists independ- ently performed the measurements on a Picture Archiving and Communication System (PACS, Philips Easy Vision PACS Viewing and Reporting Workstation with core software by SECTRA). The deep and the total cervical extensor muscles as well as the sterno- cleidomastoid were manually traced using free-form regions of interest (ROI). Each side of the neck was evaluated separately.
Measurements were obtained at the following levels, with image level being specified by using a predeter- mined labeled diagram for exact site and level with standardized planes: (i) C2 level: inferior oblique plus rectus capitis posterior major muscles (C2deep) as well as total dorsal cervical extensor muscles (C2tot; see Fig. 1b); (ii) C4 level: sternocleidomastoid muscles (C4sterno; see Fig. 1c); and (iii) C5 level: semispinalis cervicis plus multifidus plus interspinal and spinal
Figure 1. Female whiplash patient with the cross-sectional area (CSA) measurements indicated for the different muscle groups at different levels. a: Transverse STIR/TIRM (TR 4860 ms, TE 28 ms, TI 150 ms) with line markers identifying the 3 levels (C2, C4, C5), where the measurements were performed. b: Transverse STIR/TIRM (TR 5110 ms, TE 28 ms, TI 150 ms) at C2 level: deep cervical extensor muscles on both sides (left) and total dorsal cervical extensor muscles on both sides (right). c: Transverse STIR/TIRM (TR 5110 ms, TE 28 ms, TI 150 ms) at C4 level: sternocleidomastoid muscles on both sides. d: Transverse STIR/TIRM (TR 5110 ms, TE 28 ms, TI 150 ms) at C5 level: deep cervical extensor muscles on both sides (left) and total dorsal cervical extensor muscles on both sides (right).
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muscles (C5deep) as well as total dorsal cervical ex- tensor muscles (C5tot; see Fig. 1d). The middle por- tion of each vertebral body (C2, C4, C5) localized in the sagittal sequence (see Fig. 1a) was the landmark used for measurement of the CSA. The individual muscles were identified accordingly after thorough review of the anatomy. Muscle signal intensity was not reviewed as part of this substudy. All other ana- tomical structures at all cervical spinal levels were an- alyzed as part of the larger on-going study and were not part of this substudy.
Statistical Analysis
Data of both raters were averaged for descriptive anal- yses. Means and standard deviations (SD) were used to summarize the data and Pearson correlation coeffi- cients (R) were used to analyze the bivariate relation- ship of variables. Differences of CSAs between whip- lash patients and healthy controls and between women and men were analyzed with hierarchical lin- ear models for each muscle at each segmental level. Modeling procedures (17) accounted for the fact of multiple observations per subject (left and right mea- surement and two raters). Rater, age, and body mass index (BMI) nested within gender were included as cofactors and the interaction term between study group and gender was also added to all models. The rationale of using a nested effect for BMI is based on the fact that women have a lower BMI than men. Pa- rameter estimates of age and BMI were interpreted as incremental effects for each unit of change and results for categorized data (cases/controls, gender) were interpreted as differences of least-square means (LS-Means). Residual analysis showed no violation of basic assumptions for linear models and indicated a good fit of models. Intra-class correlation coefficients (ICC) were calculated to examine inter-examiner reli- ability for each measurement at each segmental level. Pearson correlation coefficients were used to detect linear relationships between muscle measurements and pain scales. The level of significance was set at P < 0.05 throughout the study, and SAS 9.1 (SAS Institute Inc., Cary, NC) was used for all calculations.
RESULTS
Demographic characteristics for the two groups (patients and controls) are shown in Table 1. No sig- nificant difference in age and BMI were seen between patients and controls and the distribution of genders across groups was identical.
Average CSA values of both raters and of the differ- ent muscle areas for patients and controls are sum- marized in Table 2. ICCs ranged from 0.52 for C2 level deep cervical extensor muscles to 0.85 for C2 level total dorsal cervical extensor muscles, indicating moderate to high agreement of measurements between the two raters. Only for two small muscle area measurements (C2 level deep muscles and C5 level deep muscles) were the values below 0.6 (usually considered as poor agreement). There was, however, an apparently systematic difference between the two raters, with rater A having smaller values with statis- tical significance for all sites with one exception. Therefore, the average of individual CSA values of both raters were used for final descriptive analysis and the rater effect was accounted for in the final sta- tistical model.
A significant correlation of 0.36 was observed between age and BMI. Correlations of individual mus- cle CSA with age and BMI are given in Table 3 and indicate moderate positive linear relationships between CSA of cervical muscles and age and BMI respectively.
Role of Gender, Age, BMI, and Localization (Left and Right) on CSA
CSA of C4 level sternocleidomastoid muscle, C5 level deep muscles, C2 level total dorsal cervical extensor muscles, and C5 level total muscle groups were sig- nificantly smaller in women than in men both in patients and controls and most CSAs increased with older age but a significant association was only seen for C2 level total muscles (Table 2). Almost all CSA increased significantly with higher BMI. No consistent patterns of effect with size of BMI on CSA were seen between males and females. No significant effects were observed whether muscles were located right or left.
CSA and Group Effect (Patient/Control)
No significant differences between patients and con- trols were observed for all muscle CSAs. Significant interaction terms were, however, observed between group and gender for C5 level deep muscles and C5 level total dorsal extensor muscles, suggesting that group effects were not consistent across men and women for these muscles, i.e., differences between genders were more prominent in controls than in cases.
Table 1
Demographic Characteristics and BMI of Patients and Controls
Controls (n ¼ 38) Patients (n ¼ 38)
F (n ¼ 19) M (n ¼ 19) MþF (n ¼ 38) F (n ¼ 19) M (n ¼ 19) MþF (n ¼ 38) P valuea
Age 31.3 38.9 35.1 31.3 39.1 35.2 ns (0.97)
BMI 22.7 23.73 23.22 22.16 23.88 23.02 ns (0.86) aTesting the hypothesis of no age and BMI difference between patients and controls.
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CSA and Clinical Symptoms
There was a significant negative correlation between patient reported pain intensity (VAS) and CSA meas- urements only for C2deep level suggesting less neck pain in patients with greater CSA of the C2deep (including the semispinalis muscle). No other signifi- cant correlations were detected. However, it is impor- tant to note that negative correlations were also seen between neck pain and CSAs of all other muscles, whereas head pain was positively correlated with all muscle CSAs with the exception of C5deep (Table 4).
DISCUSSION
In this prospective controlled study, we could not find any significant difference of muscle CSA values between patients and controls in both genders. Thus, the first hypothesis that symptomatic whiplash patients have smaller muscle areas compared with sex- and age-matched healthy asymptomatic controls as a predisposing factor is not supported. Different results may have been obtained if controls had been
acquired from the whiplash injured case group with- out consecutive symptoms. But such cases are very difficult to recruit. Moreover, there was no significant difference regarding left- and right-sided muscle measurements in all subjects. The CSAs showed no significant correlation with the pain intensity of neck pain and headache with one exception but a consist- ent tendency of less neck pain and more headache with greater CSAs.
Table 2
Overall Average CSAs with 95% confidence interval of cervical muscles across gender and study groups (average CSA values of
rater A þ B for left and right side combined)
Muscle Group Gender Mean CSAa (cm2) 95% Confidence interval
C2deep Control F 2.96 2.70–3.22
M 4.75 4.45–5.05
Overall 3.85 3.57–4.14
M 4.72 4.38–5.07
Overall 3.95 3.66–4.23
M 5.43 5.17–5.69
Overall 4.46 4.19–4.73
M 5.20 4.89–5.51
Overall 4.44 4.18–4.69
M 5.31 5.11–5.52
Overall 4.39 4.13–4.65
M 4.80 4.58–5.01
Overall 4.14 3.91–4.37
M 17.59 16.62–18.56
Overall 14.03 13.01–15.05
M 16.92 16.02–17.82
Overall 14.03 13.12–14.94
M 23.40 21.84–24.97
Overall 18.26 16.79–19.73
M 22.50 21.18–23.82
Overall 18.66 17.40–19.91
M 11.30 10.13–12.46
Overall 9.00 8.29–9.71
M 10.83 9.71–11.95
Table 3
Pearson Correlation Coefficients of Individual Muscle CSAs With
Age and BMI (Mean CSA Values of patients and Controls,…
Erika J. Ulbrich, MD,1,2* Suzanne E. Anderson, MD,2,3 Andre Busato, PhD,4
Susanne Abderhalden, MD,2,5 Chris Boesch, MD, PhD,6 Heinz Zimmermann, MD,7
Paul Heini, MD,8 Juerg Hodler, MD, PhD,5 and Matthias Sturzenegger, MD9
Purpose: To quantitatively compare the muscle cross-sec- tional areas (CSAs) of the cervical muscles in sympto- matic acute whiplash patients versus healthy controls. We hypothesized, that symptomatic whiplash patients have smaller cervical muscle CSAs than matched controls and that smaller cervical muscle CSAs in women might explain that women more frequently are symptomatic af- ter whiplash injury than men.
Materials and Methods: Prospective controlled study. Thirty-eight consecutive acute whiplash patients were examined within 48 h after a motor vehicle accident and 38 healthy age- and sex-matched controls, each half female, half male, were examined with the same protocol. MRI CSA measurements were performed of the deep and total cervical extensor muscles as well as the sternoclei- domastoid muscles using transversal STIR (Short T1 Inversion Recovery) sequences on level C2, C4, and C5 by two blinded raters. Clinical symptoms were assessed with
patient questionnaires (EuroQuol 5D, Specific Whiplash Questionnaire, head- and neck pain intensity [VAS]).
Results: Agreement of measurements between the two raters was high (intraclass correlation 0.52 to 0.85 for the different levels). No significant difference in age and body mass index were seen between patients and controls and the distribution of genders across groups was identical. There were no significant differences between patients and controls for all CSAs. Women had consistently smaller CSAs than men. The CSAs showed no significant correlation with the pain intensity of neck pain and head- ache but a consistent tendency of less neck pain and more headache with greater CSAs.
Conclusion: This small study provides no evidence that subjects with smaller CSAs of cervical extensor muscles have a higher risk in developing symptoms after a whip- lash injury and confirms smaller CSA in women.
Key Words: MRI; cross-sectional areas (CSAs); cervical extensor muscles; MRI muscle; symptomatic acute whip- lash patients J. Magn. Reson. Imaging 2011;33:668–675. VC 2011 Wiley-Liss, Inc.
NECK AND HEAD pain are the most prominent symp- toms in the acute and chronic phase after whiplash injury. The responsible tissue damage is disputed, and no consistent findings regarding for example muscle edema or hemorrhage or ligamentous tears have been confirmed (1). Factors determining whether a patient becomes symptomatic after a whiplash injury or not as reported in the literature range from the structural to psychological (2–4). As there was lit- tle available information about the effect of cervical muscle volumes on acute whiplash-associated injury, our study was designed to review this. We took a novel approach by aiming at reviewing patients within a 48-h period from the motor vehicle accident (MVA) and using as special MR imaging protocol.
Findings suggesting that cervical muscles play a role in whiplash-associated disorders (WAD) are as follows: Patients aware of an impending impact and/ or with precontracted neck muscles have less acute and chronic symptoms (5); Women are more fre- quently symptomatic than men (6,7); and Chronic
1Department of Radiology, Orthopedic University Hospital Balgrist, Zurich, Switzerland. 2Department of Diagnostic, Interventional and Pediatric Radiology, Inselspital, Bern University Hospital, and University of Bern, Switzerland. 3School of Medicine, Medical Imaging, The University of Notre Dame Sydney, Darlinghurst Campus, Australia. 4Institute for Evaluative Research in Orthopedic Surgery, University of Bern, Switzerland. 5Department of Radiology, USZ, University Hospital Zurich, Switzerland. 6Department of Clinical Research, Magnetic Resonance Spectroscopy and Methodology, University of Bern, Switzerland. 7Department of Emergency, Inselspital, Bern University Hospital, and University of Bern, Switzerland. 8Department of Orthopedics, Inselspital, Bern University Hospital, and University of Bern, Switzerland. 9Department of Neurology, Inselspital, Bern University Hospital, and University of Bern, Switzerland.
This work was performed at Department of Diagnostic, Interventional and Pediatric Radiology, Inselspital, Bern University Hospital, and University of Bern, Bern, Switzerland.
Contract grant sponsor: the Swiss National Science Foundation; Contract grant number: 405340-104531.
*Address reprint requests to: E.J.U., Orthopedic University Hospital Balgrist, Forchstrasse 340, 8008 Zurich, Switzerland. E-mail: [email protected]
Received August 4, 2010; Accepted October 20, 2010.
DOI 10.1002/jmri.22446 View this article online at wileyonlinelibrary.com.
JOURNAL OF MAGNETIC RESONANCE IMAGING 33:668–675 (2011)
CME
nloaded from https://onlinelibrary.w
nline L ibrary on [22/03/2023]. See the T
erm s and C
articles are governed by the applicable C reative C
om m
ons L icense
whiplash patients show smaller cervical spine muscle volumes and fatty infiltration compared with controls (8). However, the reduced muscle volumes in chronic whiplash patients may be a secondary phenomenon due to inactivity and these findings cannot be neces- sarily applied to investigate the role of cervical muscle volumes in the acute symptom genesis of whiplash patients.
Previous studies have reviewed whiplash patients af- ter varied time periods and documented altered mus- cle strength (9) or muscle endurance (10,11) as a con- sequence of neck pain, whether following a whiplash injury or not. Analyzing cervical range of motion does not discriminate between muscles and joints (12).
Quantitative paraspinal muscle volume assessment using cross-sectional area measurements have been performed in chronic whiplash patients and compared with healthy controls using ultrasound (13) and MRI (14,15) (females only).
This study allowed for measurements to be per- formed on muscles in consecutive acute whiplash patients (both genders) using MRI routinely within a 48-h period after MVA.
The objective of this study was to quantitatively compare the muscle cross-sectional areas (CSAs) as surrogate markers for muscle volumes of cervical ex- tensor muscles (deep and total dorsal cervical muscles at C2 and C5 level) and the sternocleidomas- toid muscles (at C4 level) at predefined multiple cervi- cal levels in symptomatic acute whiplash patients ver- sus healthy controls. Our first hypothesis was that symptomatic whiplash patients have smaller muscle areas compared with sex- and age-matched healthy asymptomatic controls as a predisposing factor. Our second hypothesis was that women are at an increased risk of being symptomatic compared with men after a whiplash injury due to smaller cervical muscle volumes.
MATERIALS AND METHODS
The responsible ethics committee and agency for au- thorization of therapeutic products approved this pro- spective study, and written informed consent was obtained from all patients and controls before study inclusion.
Subjects
Patients presenting with acute whiplash injury Grade I or II, as defined by Quebec task force (16) following a rear-end MVA with a mechanism of forceful flexion and extension of the cervical spine with persistent symptoms of at least neck pain and stiffness, were eli- gible for recruitment. A total of 76 subjects (38 con- secutive acute whiplash patients, 38 healthy controls, with half female, half male each) with an average age of 35.1 years (standard deviation [SD] 14.0 years) were recruited from the emergency department if the results for inclusion and exclusion criteria ascer- tained with standardized questionnaires where appro- priate and underwent MRI examination within 48 h
after injury. Inclusion criteria for acute whiplash patients and healthy controls included age older than 18 years and signed written informed consent. All patients were first clinically reviewed by emergency medical staff to exclude serious injury, such as unsta- ble multiple trauma, spinal fracture, and subluxation or dislocation that may necessitate immediate surgi- cal stabilization. Whiplash patients were excluded if they had a fracture or subluxation of the cervical spine as diagnosed on standard radiographs and/or computed tomography (CT), direct head injury, previ- ous surgery or neurosurgery to the head or spine, pre- vious history of whiplash with persisting pain, muscu- loskeletal inflammatory disorders or other severe illness (with continuous pain or reduction of working ability), pre-existing head and neck pain, psychiatric disorders, drug or alcohol abuse, tumor/metastases of the head and neck, claustrophobia, pacemaker, or pregnancy.
For controls, healthy asymptomatic volunteers were recruited by advertisement within the local university and were matched to patients for age and sex. The same eligibility criteria were used as for the patient group where applicable. Here, age- and sex-matched subjects having suffered a whiplash injury without consecutive symptoms would be the optimal control group, but these cases are extremely difficult to recruit for obvious reasons.
Clinical Symptoms
Symptoms in the patient group were assessed using patient questionnaires: EuroQuol 5D, Specific Whip- lash Questionnaire and visual analog scales (VAS) for head and neck pain intensity. The head and neck pain intensity scales were graded from 0 (no pain) to 100 (maximum of pain).
MRI Acquisition and Protocol
MR images were obtained using a SONATA 1.5 Tesla (T) magnet (Siemens Medical Solutions, Erlangen, Germany). All patients and healthy controls had the same MR protocol. Sagittal and transverse STIR/TIRM (Short Tau Inversion Recovery/Turbo Inversion Recov- ery Magnitude) sequences obtained as part of the larger study protocol were used for this substudy to review the muscles. The total scan time was 15 min 23 s. Parameters for the sagittal TIRM sequence con- sisted of repetition time (TR) 4860 ms, echo time (TE) 28 ms, inversion time 150 ms, flip angle 180, turbo factor 7, total acquisition time 5 min 47 s. Two trans- versal TIRM sequences with TR 5110 ms, TE 28 ms, inversion time 150 ms, flip angle 180, turbo factor 7, and total acquisition time 4 min 48 s each were com- bined to cover the region of interest. All images were acquired on a 512 256 pixel matrix with a 210 mm 158 mm field of view and a slice thickness of 3 mm. A dedicated neck coil and a spine array coil were used with the patient in the supine position. Saturation pulses placed over the upper airway region were used for fat/water suppression and to remove flow artifacts.
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Sagittal and transverse slices of the cervical spine were obtained from the midpoint of the cerebellum through to the second thoracic vertebral level to include the entire cervical extensor musculature. The 19 sagittal images were centered on the spinal cord at the C4 level. The 20 transverse images per slab were planned on the sagittal sequence and were performed with two overlapping slabs which were perpendicular to the posterior surface of the vertebral body in the middle of the respective slab. Three slabs were used, if required, to cover the entire region. The tilt of the transverse images was thus adapted to the vertebral body orientation. Each transverse slab included 20 images.
Imaging Analysis
Muscle CSA were taken as surrogate markers for muscle volumes (14,15), instead of doing muscle vol-
umes, to be in line with previous investigations to allow for review. Two blinded radiologists independ- ently performed the measurements on a Picture Archiving and Communication System (PACS, Philips Easy Vision PACS Viewing and Reporting Workstation with core software by SECTRA). The deep and the total cervical extensor muscles as well as the sterno- cleidomastoid were manually traced using free-form regions of interest (ROI). Each side of the neck was evaluated separately.
Measurements were obtained at the following levels, with image level being specified by using a predeter- mined labeled diagram for exact site and level with standardized planes: (i) C2 level: inferior oblique plus rectus capitis posterior major muscles (C2deep) as well as total dorsal cervical extensor muscles (C2tot; see Fig. 1b); (ii) C4 level: sternocleidomastoid muscles (C4sterno; see Fig. 1c); and (iii) C5 level: semispinalis cervicis plus multifidus plus interspinal and spinal
Figure 1. Female whiplash patient with the cross-sectional area (CSA) measurements indicated for the different muscle groups at different levels. a: Transverse STIR/TIRM (TR 4860 ms, TE 28 ms, TI 150 ms) with line markers identifying the 3 levels (C2, C4, C5), where the measurements were performed. b: Transverse STIR/TIRM (TR 5110 ms, TE 28 ms, TI 150 ms) at C2 level: deep cervical extensor muscles on both sides (left) and total dorsal cervical extensor muscles on both sides (right). c: Transverse STIR/TIRM (TR 5110 ms, TE 28 ms, TI 150 ms) at C4 level: sternocleidomastoid muscles on both sides. d: Transverse STIR/TIRM (TR 5110 ms, TE 28 ms, TI 150 ms) at C5 level: deep cervical extensor muscles on both sides (left) and total dorsal cervical extensor muscles on both sides (right).
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muscles (C5deep) as well as total dorsal cervical ex- tensor muscles (C5tot; see Fig. 1d). The middle por- tion of each vertebral body (C2, C4, C5) localized in the sagittal sequence (see Fig. 1a) was the landmark used for measurement of the CSA. The individual muscles were identified accordingly after thorough review of the anatomy. Muscle signal intensity was not reviewed as part of this substudy. All other ana- tomical structures at all cervical spinal levels were an- alyzed as part of the larger on-going study and were not part of this substudy.
Statistical Analysis
Data of both raters were averaged for descriptive anal- yses. Means and standard deviations (SD) were used to summarize the data and Pearson correlation coeffi- cients (R) were used to analyze the bivariate relation- ship of variables. Differences of CSAs between whip- lash patients and healthy controls and between women and men were analyzed with hierarchical lin- ear models for each muscle at each segmental level. Modeling procedures (17) accounted for the fact of multiple observations per subject (left and right mea- surement and two raters). Rater, age, and body mass index (BMI) nested within gender were included as cofactors and the interaction term between study group and gender was also added to all models. The rationale of using a nested effect for BMI is based on the fact that women have a lower BMI than men. Pa- rameter estimates of age and BMI were interpreted as incremental effects for each unit of change and results for categorized data (cases/controls, gender) were interpreted as differences of least-square means (LS-Means). Residual analysis showed no violation of basic assumptions for linear models and indicated a good fit of models. Intra-class correlation coefficients (ICC) were calculated to examine inter-examiner reli- ability for each measurement at each segmental level. Pearson correlation coefficients were used to detect linear relationships between muscle measurements and pain scales. The level of significance was set at P < 0.05 throughout the study, and SAS 9.1 (SAS Institute Inc., Cary, NC) was used for all calculations.
RESULTS
Demographic characteristics for the two groups (patients and controls) are shown in Table 1. No sig- nificant difference in age and BMI were seen between patients and controls and the distribution of genders across groups was identical.
Average CSA values of both raters and of the differ- ent muscle areas for patients and controls are sum- marized in Table 2. ICCs ranged from 0.52 for C2 level deep cervical extensor muscles to 0.85 for C2 level total dorsal cervical extensor muscles, indicating moderate to high agreement of measurements between the two raters. Only for two small muscle area measurements (C2 level deep muscles and C5 level deep muscles) were the values below 0.6 (usually considered as poor agreement). There was, however, an apparently systematic difference between the two raters, with rater A having smaller values with statis- tical significance for all sites with one exception. Therefore, the average of individual CSA values of both raters were used for final descriptive analysis and the rater effect was accounted for in the final sta- tistical model.
A significant correlation of 0.36 was observed between age and BMI. Correlations of individual mus- cle CSA with age and BMI are given in Table 3 and indicate moderate positive linear relationships between CSA of cervical muscles and age and BMI respectively.
Role of Gender, Age, BMI, and Localization (Left and Right) on CSA
CSA of C4 level sternocleidomastoid muscle, C5 level deep muscles, C2 level total dorsal cervical extensor muscles, and C5 level total muscle groups were sig- nificantly smaller in women than in men both in patients and controls and most CSAs increased with older age but a significant association was only seen for C2 level total muscles (Table 2). Almost all CSA increased significantly with higher BMI. No consistent patterns of effect with size of BMI on CSA were seen between males and females. No significant effects were observed whether muscles were located right or left.
CSA and Group Effect (Patient/Control)
No significant differences between patients and con- trols were observed for all muscle CSAs. Significant interaction terms were, however, observed between group and gender for C5 level deep muscles and C5 level total dorsal extensor muscles, suggesting that group effects were not consistent across men and women for these muscles, i.e., differences between genders were more prominent in controls than in cases.
Table 1
Demographic Characteristics and BMI of Patients and Controls
Controls (n ¼ 38) Patients (n ¼ 38)
F (n ¼ 19) M (n ¼ 19) MþF (n ¼ 38) F (n ¼ 19) M (n ¼ 19) MþF (n ¼ 38) P valuea
Age 31.3 38.9 35.1 31.3 39.1 35.2 ns (0.97)
BMI 22.7 23.73 23.22 22.16 23.88 23.02 ns (0.86) aTesting the hypothesis of no age and BMI difference between patients and controls.
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CSA and Clinical Symptoms
There was a significant negative correlation between patient reported pain intensity (VAS) and CSA meas- urements only for C2deep level suggesting less neck pain in patients with greater CSA of the C2deep (including the semispinalis muscle). No other signifi- cant correlations were detected. However, it is impor- tant to note that negative correlations were also seen between neck pain and CSAs of all other muscles, whereas head pain was positively correlated with all muscle CSAs with the exception of C5deep (Table 4).
DISCUSSION
In this prospective controlled study, we could not find any significant difference of muscle CSA values between patients and controls in both genders. Thus, the first hypothesis that symptomatic whiplash patients have smaller muscle areas compared with sex- and age-matched healthy asymptomatic controls as a predisposing factor is not supported. Different results may have been obtained if controls had been
acquired from the whiplash injured case group with- out consecutive symptoms. But such cases are very difficult to recruit. Moreover, there was no significant difference regarding left- and right-sided muscle measurements in all subjects. The CSAs showed no significant correlation with the pain intensity of neck pain and headache with one exception but a consist- ent tendency of less neck pain and more headache with greater CSAs.
Table 2
Overall Average CSAs with 95% confidence interval of cervical muscles across gender and study groups (average CSA values of
rater A þ B for left and right side combined)
Muscle Group Gender Mean CSAa (cm2) 95% Confidence interval
C2deep Control F 2.96 2.70–3.22
M 4.75 4.45–5.05
Overall 3.85 3.57–4.14
M 4.72 4.38–5.07
Overall 3.95 3.66–4.23
M 5.43 5.17–5.69
Overall 4.46 4.19–4.73
M 5.20 4.89–5.51
Overall 4.44 4.18–4.69
M 5.31 5.11–5.52
Overall 4.39 4.13–4.65
M 4.80 4.58–5.01
Overall 4.14 3.91–4.37
M 17.59 16.62–18.56
Overall 14.03 13.01–15.05
M 16.92 16.02–17.82
Overall 14.03 13.12–14.94
M 23.40 21.84–24.97
Overall 18.26 16.79–19.73
M 22.50 21.18–23.82
Overall 18.66 17.40–19.91
M 11.30 10.13–12.46
Overall 9.00 8.29–9.71
M 10.83 9.71–11.95
Table 3
Pearson Correlation Coefficients of Individual Muscle CSAs With
Age and BMI (Mean CSA Values of patients and Controls,…
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