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Musculoskeletal Imaging |
1 From the Departments of Radiology (C.W.A.P., C.A.B., M.Z., J.H.) and Orthopedic Surgery (N.B.), Orthopedic University Hospital, Balgrist, Forchstrasse 340, CH-8008 Zurich, Switzerland. From the 1999 RSNA scientific assembly. Received February 16, 2000; revision requested March 28; revision received April 20; accepted May 22. Supported by a Schweizerische Unfallversicherungsanstalt, Lucerne, Switzerland, grant. Address correspondence to C.W.A.P. (e-mail: pfirrm16@centralnet.ch).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Fifty healthy individuals (31 men, 19 women) with a mean age of 30 years (range, 19–47 years) underwent coronal T1- and T2-weighted and transverse T1-weighted MR imaging. MR findings were analyzed independently by two musculoskeletal radiologists, with disagreements resolved in conference.
RESULTS: Alar ligaments were detected in 42 (84%) (left side) and 38 (76%) (right side) of 50 individuals. The majority of ligaments (88%) and joints (58%) of the craniocervical junction (CCJ) were asymmetric. Asymmetry of the joint between C1 and C2 was less frequent (46%). Small amounts of fluid were detected in 8% of CCJ joints and 56% of C1-C2 joints in asymptomatic individuals.
CONCLUSION: Asymmetry of alar ligaments, CCJ and C1-C2 facet joints, and joint effusions are common in asymptomatic individuals. The clinical relevance of these MR findings is therefore limited in the identification of the source of neck pain in symptomatic patients.
Index terms: Atlas and axis, 31.121411, 31.40, 319.121412 • Ligaments, injuries, 319.40 • Ligaments, MR, 319.121411, 319.121412 • Neck, anatomy, 31.121411 • Neck, injuries, 31.40 • Neck, MR, 31.121411, 319.121412
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Debate continues on the clinical relevance of structural alterations of the alar ligaments and articular structures (4,5) in the upper cervical spine as a source of neck pain after whiplash injuries. Direct visualization of the alar ligaments with computed tomography (CT) has been proposed as a diagnostic tool (6), although soft-tissue contrast may be insufficient for this purpose (7). Later experimental findings (8) have demonstrated that lesions of the alar ligaments result in an increased range of rotation to the contralateral side. Rotation measurements by using CT in maximum right and left rotation of the head have been advocated for indirect detection of alar ligament lesions (9). Therefore, magnetic resonance (MR) imaging has been used for direct visualization of the alar ligaments and the craniocervical junction (CCJ) (7,10). Detection of artificial lesions of cadaveric alar ligaments with MR imaging has been promising (7).
The assessment of symptomatic patients with whiplash injuries should be based on a thorough knowledge of structural alterations of the alar ligaments and articular joints in the upper cervical spine in asymptomatic individuals. So far, to our knowledge, this issue has not been comprehensively addressed. In assessing the MR morphology of the alar ligaments and articular joints in the upper cervical spine, we hypothesized that structural alterations of the alar ligaments and articular joints (ie, CCJ and C1-C2) are frequent findings in asymptomatic individuals that limit their clinical relevance in the identification of the source of neck pain in symptomatic patients. Thus, the objective of this investigation was to assess the MR appearance of the alar ligaments and joints in the upper cervical spine to determine the prevalence of structural alterations in asymptomatic individuals.
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MATERIALS AND METHODS |
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MR Imaging Protocol
MR imaging was performed with a 1.0-T unit (Impact Expert; Siemens Medical Systems, Erlangen, Germany) with a dedicated receive-only cervical spine coil. Imaging parameters and planes were optimized for this unit in 10 volunteers (six men, four women) with a mean age of 32 years (range, 24–38 years). The examinations in these 10 volunteers were used only for optimizing the imaging parameters. No further data were collected at these examinations. The tested sequences included two-dimensional gradient-echo, three-dimensional gradient-echo, and spin-echo sequences. The following imaging parameters were varied: section thickness (2–5 mm), field of view (8 x 6 cm to 16 x 13 cm), and matrix size (256 x 180 to 512 x 256). The imaging quality of the sequences was judged subjectively by three radiologists (C.W.A.P., M.Z., J.H.) in consensus.
The following parameters resulted from this preliminary investigation: Examinations were performed with the patient supine and the head fixed in neutral position. Neutral position of the head was verified on a transverse localizer image. A line drawn through the nasal septum and internal occipital crista had to be perpendicular to the imaging table. Two T1-weighted spin-echo images (350/15 [repetition time msec/echo time msec], three signals acquired) with both 3- and 4-mm section thicknesses and one T2-weighted turbo spin-echo image (4,000/130, four signals acquired) with a 4-mm section thickness were obtained in a coronal plane parallel to the dens. The field of view was 26 x 13 cm, and the imaging matrix was 512 x 180. T1-weighted transverse images were obtained from the base of the skull, including the entire dens. Imaging parameters were 740/12, 3-mm-thick sections, 18-cm field of view, 256 x 192 image matrix, and four signals acquired.
Analysis of MR Images
The images were read by two musculoskeletal radiologists (C.W.A.P., M.Z.) independently. All sequences were available for analysis. The MR images were graded in terms of the depiction of the alar ligaments and were classified as well defined with regular contour, well defined with irregular contour, or not differentiable from surrounding tissue. The signal intensity of the alar ligaments in comparison with that of adjacent muscle tissue was determined on T1- and T2-weighted images and was classified as isointense, hypointense, or hyperintense. The signal intensity was further classified as homogeneous or heterogeneous. The superior and inferior borders of the alar ligaments were described as parallel, convergent, or divergent to the periphery. The course of the ligaments was described as horizontal, upward, or downward and as symmetric or asymmetric. The position of the dens was analyzed by means of inspection and classified as centered or deviated to the left or right with regard to the lateral masses of C1.
Symmetry of the CCJ and C1-C2 facet joints was determined by means of qualitative left-to-right comparison of joint angulation, shape, and size. The presence of CCJ and C1-C2 facet joint effusions was analyzed on T2-weighted images. The presence of joint effusion was defined as a collection of fluid within the joint space. Interobserver disagreements at the independent evaluations were resolved in conference.
Statistical Analysis
The prevalence of the findings was calculated for both readers. Interobserver agreement was measured by using the 
statistic (12). The agreement was rated as follows: A value of between 0 and 0.20 indicated slight agreement; between 0.21 and 0.40, fair agreement; between 0.41 and 0.60, moderate agreement; between 0.61 and 0.80, substantial agreement; and 0.81 or greater, excellent agreement (12). 
2 tests were used to evaluate the relationship between findings. A P value of less than .05 was considered to indicate a statistically significant difference.
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RESULTS |
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The shape of most ligaments was convergent to the periphery (76% left and 68% right). In 24% (left) and 32% (right) of the individuals, ligament borders were parallel. No divergent ligament forms were detected. The orientation of the ligaments was caudocranial in 41% and 47%, horizontal in 52% and 47%, and craniocaudal in 7% and 5% on the left and right, respectively. In the majority (88%) of the individuals, the ligaments were asymmetric (Figs 2, 3).
The dens was deviated to the left in 14% individuals and to the right in 12% of the individuals. There was left-to-right asymmetry in 58% of the CCJ joints. Asymmetry of C1-C2 facet joints was less frequent (46%). Small amounts of fluid were detected in 4% and 4% of the CCJ and in 36% and 48% of the C1-C2 facet joints (Fig 5) on the left and right, respectively. Alar asymmetry correlated with CCJ joint asymmetry (P = .002) but not with C1-C2 asymmetry (P = .12). No other significant correlation was found between alar ligament asymmetry and sex, age, dens position, or fluid in the CCJ and C1-C2 joints.
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value for interobserver correlation of all findings varied between 0.37 and 0.82 (Tables 1–3). |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The alar ligaments connect the lateral aspect of the dens and the medial inferior aspect of the occipital condyles (6). Some investigators (8,13) report an additional inconstant ligamentous attachment to the lateral mass of the atlas. On the basis of anatomic study findings, the mean length of the alar ligaments is 11 mm cranially and 13 mm caudally, and the mean area is 3.2 x 6.0 mm (4), with the larger diameter found in the craniocaudal direction. The orientation of the alar ligaments is highly variable (14). In the coronal plane, ligaments may be orientated horizontally or may be tilted in a slight craniocaudal or caudocranial direction. The orientation depends on the length of the dens. The mean angle between the two ligaments is 140°–180° in the coronal plane (4,14).
In terms of the orientation of the ligaments, our results are in line with those of the aforementioned studies in cadavers and symptomatic patients. In approximately one-half of our individuals, the alar ligaments were oriented caudocranially, and in the other half, they were oriented horizontally. Craniocaudal orientation was rare. On T1-weighted spin-echo and T2-weighted turbo spin-echo images, the signal intensity of the alar ligaments was the same as that of muscle tissue in the majority of individuals. However, there was also a relevant number of hyperintense (21% left and right) and hypointense (14% left and 21% right) ligaments and a heterogeneous signal intensity in our asymptomatic population. Therefore, signal intensity criteria are probably difficult to use for the diagnosis of alar ligament alterations.
The alar ligaments were detected unequivocally in the majority of the asymptomatic individuals (84% left and 76% right). On continuous coronal sections with 3-mm section thickness, the ligament was usually visible on one or two images. A smaller number of ligaments (16% left and 24% right) were not clearly differentiated from surrounding tissue. This finding is probably explained by the fact that some individuals had only small amounts of epidural fat and that there was a close relationship between the alar ligaments and structures with similar MR signal intensity (joint capsules, transverse and cruciate ligaments, and the tectorial membrane).
In a previously published MR study (7), the alar ligament was detected in all cases. The detection rate was somewhat lower in our study, but the results of the aforementioned study were based on findings in only eight cases. The choice of sequence (three-dimensional gradient-echo) may play a role with regard to this difference. However, on the basis of the findings of our preliminary test series, gradient-echo sequences resulted in lower image quality compared with that of spin-echo sequences. Throughout the study, all sequences were made available. In our experience, the coronal images were the most important because they often show the alar ligaments in their entire course. Although the value of the T1-weighted transverse images was limited, they provided important information to define the position of the dens and to confirm the neutral position of the head.
Almost all the values for interobserver agreement regarding the evaluation of the alar ligaments and occipitoatlantoaxial joints ranged from moderate to substantial ( = 0.45–0.73) (Tables 1–3). There was only one excellent value ( = 0.82) for the homogeneity of the right alar ligament. The value ( = 0.37) for the presence of joint effusion in the right CCJ was fair. This finding was most likely caused by the low frequency (left, n = 2; right, n = 3) (12).
The main function of the alar ligaments is to limit rotation to the contralateral side. It has been shown experimentally (8) that a tear of the alar ligament results in a higher range of motion to the contralateral side. Rotational instability may result from such injury. According to the literature (4,8), there is a possibility of tearing of the alar ligaments in a whiplash injury that occurs with the head in a rotated position. Experimental study findings (5) have shown the lower strength of the alar ligaments compared with that of the other ligaments of the CCJ and, therefore, their higher vulnerability. However, most reports (15) of complete alar ligament tears refer to fatalities with concomitant injuries to neural structures and the cervical spine. Experimental disruptions in cadavers were detected on MR images (7).
Lesions of the alar ligament with or without associated rotational instability have been discussed (8,16) as one possible cause of whiplash-associated disorders. Structural alterations related to acute whiplash injury are rarely seen (17). However, MR studies of the cervical spine after whiplash injury have not specifically addressed the alar ligaments. One possible approach to the indirect diagnosis of ligamentous or capsular tears related to whiplash injury is an assessment of the CCJ at rotational CT (9). Because of the substantial variability of such rotational measurements, this method has remained controversial and has not found widespread acceptance (7).
Direct visualization of alar ligament alterations or indirect signs of capsular injury, such as articular joint effusions, would be of diagnostic and medicolegal interest, when the substantial socioeconomic effect of whiplash injury is considered (1). On the basis of these study results, MR imaging is limited in the identification of structural alterations in symptomatic patients with whiplash-associated disorders because of the high prevalence of alar ligament and articular joint asymmetry in asymptomatic subjects. The majority (88%) of alar ligaments are asymmetric in asymptomatic individuals. Therefore, alar asymmetry in symptomatic patients appears not to be a reliable indicator for a source of pain. Furthermore, the CCJ and C1-C2 joints were asymmetric in 58% and 46% of individuals, respectively. Such variability must be taken into account when rotational measurements of the craniocervical region is performed with CT or MR imaging. A small amount of fluid, which represents a potential sign of capsular injury, was frequent (56%) in the C1-C2 facet joints and therefore should not be classified as abnormal.
In conclusion, these study findings have verified our initial hypothesis that structural alterations of the alar ligaments and articular joints (ie, CCJ and C1-C2) are frequent findings in asymptomatic individuals that limit their clinical relevance in the identification of the source of neck pain in symptomatic patients.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, C.W.A.P.; study concepts, C.W.A.P., N.B., J.H.; study design, C.W.A.P.; definition of intellectual content, M.Z., C.W.A.P., J.H.; literature research, C.W.A.P.; clinical studies, C.W.A.P., C.A.B.; data acquisition, C.W.A.P., C.A.B.; data analysis, C.W.A.P., M.Z.; statistical analysis, C.W.A.P., J.H.; manuscript preparation, C.W.A.P.; manuscript editing, J.H.; manuscript review, J.H., N.B.; manuscript final version approval, J.H.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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This article has been cited by other articles:
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  K.-B. Sim and J.K. Park A nodular calcification of the alar ligament simulating a fracture in the craniovertebral junction. AJNR Am. J. Neuroradiol., October 1, 2006; 27(9): 1962 - 1963. [Abstract] [Full Text] [PDF]
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