Diagnostic Benefit of MRI for Exclusion of Ligamentous Injury in Patients with Lateral Atlantodental Interval Asymmetry at Initial Trauma CT
Abstract
Background
Cervical spine CT is regularly performed to exclude cervical spine injury during the initial evaluation of trauma patients. Patients with asymmetry of the lateral atlantodental interval (LADI) often undergo subsequent MRI to rule out ligamentous injuries. The clinical relevance of an asymmetric LADI and the benefit of additional MRI remain unclear.
Purpose
To evaluate the diagnostic benefit of additional MRI in patients with blunt trauma who have asymmetry of the LADI and no other cervical injuries.
Materials and Methods
Patients who underwent cervical spine CT during initial trauma evaluation between March 2017 and August 2019 were retrospectively evaluated. Those who underwent subsequent MRI because of LADI asymmetry of 1 mm or greater with no other signs of cervical injury were identified and reevaluated by two readers blinded to clinical data and initial study reports regarding possible ligamentous injuries.
Results
Among 1553 patients, 146 (9%) had LADI asymmetry of 1 mm or greater. Of these, 46 patients (mean age ± standard deviation, 39 years ± 22; 28 men; median LADI asymmetry, 2.4 mm [interquartile range, 1.8–3.1 mm]) underwent supplementary MRI with no other signs of cervical injury at initial CT. Ten of the 46 patients (22%) showed cervical tenderness at clinical examination, and 36 patients (78%) were asymptomatic. In two of the 46 patients (4%), MRI revealed alar ligament injury; both of these patients showed LADI asymmetry greater than 3 mm, along with cervical tenderness at clinical examination, and underwent treatment for ligamentous injury. In 13 of the 46 patients (28%), signal intensity alterations of alar ligaments without signs of rupture were observed. Four of these 13 patients (31%) were subsequently treated for ligamentous injury despite being asymptomatic.
Conclusion
Subsequent MRI following CT of the cervical spine in trauma patients with lateral atlantodental interval asymmetry may have diagnostic benefit only in symptomatic patients. In asymptomatic patients without proven cervical injuries, subsequent MRI showed no diagnostic benefit and may even lead to overtreatment.
© RSNA, 2021
Summary
Additional MRI for exclusion of ligamentous injuries in trauma patients with lateral atlantodental interval asymmetry provides diagnostic benefit in symptomatic patients only and may contribute to overtreatment in asymptomatic patients.
Key Results
■ In a retrospective study of 1553 trauma patients, 146 (9%) showed lateral atlantodental interval (LADI) asymmetry of 1 mm or greater, with no correlation to head rotation or lateral head tilt.
■ Two of 46 patients (4%) with LADI asymmetry and lack of proven cervical injury at CT showed alar ligament injury at MRI and were symptomatic.
■ Normal-variant signal intensity alterations of the alar ligaments were misinterpreted as ligamentous injury in asymptomatic patients, resulting in unnecessary treatment.
Introduction
Up to 2%–6% of patients show acute cervical spine injuries (CSIs) after blunt trauma (1,2). Most CSIs are reported to be fractures; ligamentous injuries and combined injuries are far less common (2), and spinal cord injuries occur rarely (0.07%–0.26%) (3). However, if such lesions are missed during the initial clinical examination, serious neurologic deficits and cervical spine instability may arise. Previous studies have shown that about half of all CSIs are not suspected at clinical examination. Thus, criteria suggesting CSIs have been established as a decision aid for the use of further radiologic evaluation (eg, the National Emergency X-Radiography Utilization Study Group, or NEXUS, criteria and the Canadian C-Spine Rule) (4). On the basis of those criteria, guidelines such as the American College of Radiology Appropriateness Criteria (5) and the Eastern Association for the Surgery of Trauma Practice Management Guidelines (6) recommend further radiologic evaluation following adequate cervical trauma. CT has replaced conventional radiography as the modality of choice because of its superiority in the detection of skeletal injuries (7). Hence, CT is frequently used for initial evaluation of trauma patients in the emergency department because it is fast and accurate, has widespread availability, and is cost-effective (8).
The exclusion of ligamentous injury at cervical spine CT (CSCT) may cause diagnostic difficulties. Although an increased anterior atlantodental interval (AADI) is accepted as a sign of underlying pathologic abnormality (9), the clinical relevance of an asymmetric lateral atlantodental interval (LADI) remains unclear. Besides ligamentous injury or atlantoaxial rotational fixation and/or subluxation at the C1/C2 level (10,11), anatomic variations, head rotation, and muscle spasm may also affect LADI. Hence, LADI asymmetry may also be observed in healthy individuals as a normal variant (12,13). Trauma patients with LADI asymmetry at radiography or CT are frequently admitted for subsequent MRI to rule out CSI. This leads to a tremendous amount of MRI examinations that occupy MRI resources and may also increase treatment costs. Previous studies have shown ambiguous results concerning the benefit of additional MRI after negative findings at CSCT (14–18).
The purpose of this study was to assess the additional diagnostic value of cervical spine MRI in trauma patients with detected LADI asymmetry as the only abnormality at preceding CSCT.
Materials and Methods
The study was approved by the institutional review board, and the need for written informed consent was waived because of the retrospective study design.
Patient Selection
We evaluated patients who presented to the emergency department of the University Hospital Bonn, Germany, who underwent CSCT after being involved in blunt trauma between March 2017 and August 2019. Inclusion criteria were (a) proof of an LADI asymmetry of 1 mm or more at the preceding CSCT examination without any other radiologic signs of CSI and (b) subsequent MRI due to LADI asymmetry. Exclusion criteria were (a) no LADI asymmetry at CSCT, (b) pathologic findings at CSCT, (c) previous cervical surgery, or (d) no additional MRI performed. Patient characteristics were retrieved by using the institutional clinical information system.
Image Acquisition
All CT scans were obtained in the emergency department of our hospital by using a 128-section CT scanner (Somatom Definition Edge with Sliding Gantry; Siemens Healthcare). Noncontrast CT scans were obtained with a collimation of 128 × 0.6 mm and a pitch of 0.8. Reformatted images were reconstructed with a section thickness of 1 mm in coronal, transverse, and sagittal planes. X-CARE (Siemens Healthcare) was used as the tube current modulation technique.
Noncontrast MRI examinations were performed with either a 1.5-T or 3.0-T whole-body MRI system (Ingenia; Philips Healthcare). In addition to a sagittal T1-weighted turbo spin-echo sequence, T2-weighted mDIXON turbo spin-echo sequences in coronal, sagittal, and axial planes were performed. Typical imaging parameters are given in Tables E1 and E2 (online).
Image Analysis
CT and MRI scans of included patients were reevaluated by two independent board-certified readers (J.A.L. and P.A.K., with 8 and 9 years of experience, respectively, in CT and MRI trauma imaging) with regard to ligamentous injuries and any other radiologic signs of CSI. In case of discrepancy, a consensus reading was held. The results of the expert reading were considered the reference standard against which the results of the initial report were compared. All measurements were performed by the same radiologist (C.H.E., with 4 years of experience in CT and MRI trauma imaging). All readers were blinded to clinical data and initial study reports but not to the indication for MRI.
Image analysis was performed at a dedicated workstation (IMPAX EE; AGFA Healthcare). For the CT scans, axial, coronal, and sagittal reformations were reconstructed to allow maximal symmetry. AADI, LADI, head rotation, lateral head tilt, and lateral translation of the lateral margins of C1 on C2 were calculated.
For determining the AADI, sagittal reconstructions were used, measuring in midsagittal planes. Each individual left and right LADI and the offset of the lateral margins of C1 on C2 were measured in the coronal plane (see Fig E1 [online] for exemplary measurements).
LADI asymmetry was calculated by subtracting the value of the left interspace from the right interspace. The values were noted in absolute and real numbers to determine the magnitude and directionality of the asymmetry.
The lateral head tilt was measured in coronal CT reconstructions. For C0 lateral tilt, a line between the most caudal points of the occipital condyles was drawn and the angle to a reference line parallel to the CT table calculated. C2 lateral tilt was measured by determining the angle between the horizontal center line of axis vertebrae and the reference line parallel to the CT table. The differences of the respective angles were calculated.
Rotational angles of the occiput and of the atlas and axis vertebrae were measured in axial reconstructions in correlation to a vertical reference line (perpendicular to the CT table), and the differences of angles between C0, C1, and C2 were calculated.
Statistical Analysis
Statistical analysis was performed by one author (J.A.L.) using Prism software (version 8.4.2,; GraphPad Software). Normal distribution was checked by using the Shapiro-Wilk test. Continuous variables were summarized with medians and interquartile ranges (IQRs) or ranges or with means ± standard deviations, as appropriate. Continuous variables were compared by using the Mann-Whitney U test or Student t test, as appropriate. Dichotomous variables were summarized with counts and percentages and were compared between respective groups by using the χ2 test. Correlation was tested with the Spearman correlation coefficient. Interrater agreement of the two musculoskeletal expert readers was determined by using the Cohen κ coefficient. P < .05 was considered to represent a statistically significant difference.
Results
Patient Characteristics
A total of 1553 trauma patients underwent CSCT in the emergency department of our hospital between March 2017 and October 2019. Among these, 1407 patients were excluded for lack of LADI asymmetry of 1 mm or greater, leaving 146 of the 1553 patients (9%) in the study sample. Among those 146 patients, 62 (43%) underwent supplementary MRI of the cervical spine to exclude CSI. Among those, another 16 patients had to be excluded because there were pathologic findings on the initial CT scan (n = 13) or the patient had previously undergone cervical surgery (n = 3). Thus, 46 of the 62 patients (74%) with asymmetry of the LADI as the only radiologic sign of potential pathologic abnormality at CT were included (Fig 1). The median time between CT and MRI was 1 day (IQR, 1–3.3 days). Twenty-eight of the 46 patients (61%) underwent 1.5-T imaging and 18 (39%) underwent 3.0-T imaging (P = .06). The mean patient age was 39 years ± 22 (standard deviation); 28 patients were men (mean age, 42 years ± 23) and 18 were women (mean age, 32 years ± 20) (P = .14). Forty-two of the 46 patients (91%) presented to the emergency department with a pre–clinically applied hard collar. The primary indication for MRI in these patients was exclusion of ligamentous injuries due to an asymmetry of the LADI at trauma CT. A more detailed overview of the patient characteristics and indications is given in Table 1.
Clinical Examination
Ten of the 46 patients (22%) presented with cervical tenderness on palpation at initial clinical examination (first and/or second survey). Two symptomatic patients had ligamentous injury of the alar ligaments with influence on the treatment regimen. One symptomatic patient had a prevertebral hematoma and another had an interspinous ligament strain; this had no influence on the treatment regimen of either patient. Six symptomatic patients did not show CSI at MRI. Thirty-six of the 46 patients (78%) did not show any clinical symptoms at initial clinical examination.
CT Results
The median AADI was 1.3 mm (IQR, 1.0–1.5 mm). The median right-sided LADI was 3.7 mm (IQR, 2.8–5.1 mm), and the median left-sided LADI was 4.2 mm (IQR, 2.7–5.8 mm). The median LADI asymmetry was 2.4 mm (IQR, 1.8–3.1 mm); asymmetry was right-sided in 27 of the 46 patients (59%) (see Tables 2 and 3 for detailed magnitudes of LADI asymmetry). The median head rotation was 2.3° (IQR, 1.4°–5.1°), mostly with rotation toward the right side (24 of 46 patients [52%]). The median lateral tilt was 1.8° (IQR, 0.6°–3.3°). No correlation was observed between LADI asymmetry and head rotation (r = –0.13,; P = .38) or lateral head tilt (r = 0.07; P = .66) (Fig 2). The lateral margins of C1 on C2 showed a median lateral translation of 2.7 mm (IQR, 2.4–3.0 mm) on the right side and 2.7 mm (IQR, 2.4–2.9 mm) on the left side. No patients showed a loss of C1/C2 facet overlap less than 20% as an indicator of rotatory subluxation.
MRI Results
Six of the 46 patients with LADI asymmetry and lack of cervical injuries at initial CSCT (13%) showed CSI at MRI (Table 1). Ligamentous injuries of the cervical spine at the C1/C2 level were verified in two of the 46 patients (4%); one patient had a complete rupture of the right alar ligament (LADI asymmetry, 5.1 mm; Fig 3), and the other had a partial rupture of the right alar ligament (LADI asymmetry, 3.4 mm; Fig 4). The diagnoses influenced the therapeutic regimen in both patients: surgical fixation of the C1/C2 joint was needed for the first patient, and a 6-week extension of cervical collar treatment was needed for the other patient. Apart from those ligamentous injuries, an interspinous ligament strain at the C6/C7 level (n = 1, symptomatic patient), mild bone bruises (n = 2, both patients asymptomatic), and a prevertebral hematoma (n = 1, symptomatic patient) were diagnosed in the remaining four patients with CSI. These findings did not necessitate any treatment. Signal intensity alterations of the alar ligaments without ruptures or with partial ruptures were observed in 13 of the 46 patients (28%) (Fig 5). In four of the 46 patients (9%), signal intensity alterations were considered as ligamentous injuries at the initial clinical reading but not at consensus review by the two expert readers. This initial evaluation led to an adjustment of treatment regimen by extending the use of a cervical collar for 6 weeks. These patients were asymptomatic. The κ coefficient of the two expert readers regarding the evaluation of spine MRI before consensus reading was good (κ = 0.79; 95% CI: 0.39, 1.0).
Discussion
Until now, studies investigating the utility of MRI in the detection of cervical spine injuries after a negative CT scan have shown ambiguous results (14–18). Trauma society guidelines recommend cervical collar removal after a negative CT scan alone, even in adults with obtunded blunt trauma (19). Because lateral atlantodental interval asymmetry in trauma patients can be caused by normal variants, ligamentous injuries, and incorrect positioning, such a finding may lead to diagnostic difficulties at cervical spine CT.
Our study aimed to clarify whether trauma patients with LADI asymmetry and lack of cervical injuries at initial CT benefit from complementary MRI. We found an LADI asymmetry of 1 mm or greater in 146 of 1553 trauma patients (9%), with no correlation to head rotation (r = –0.13; P = .38) or lateral head tilt (r = 0.07; P = .66). Six of the 46 patients (13%) with supplementary MRI had CSI; however, only two of these patients (4%) had unilateral alar ligament injuries that resulted in a therapeutic consequence. Both patients were symptomatic, which already clinically suggested a ligamentous injury. No other patients had ligamentous injuries, even if larger LADI asymmetry (up to 7.1 mm) was present. Most patients (36 of 46 [78%]) were asymptomatic at the cervical level. Thirteen of the 46 patients (28%) showed at least one-sided signal intensity alterations of the alar ligaments without ruptures as a normal variant; only two patients were symptomatic. These signal intensity alterations were initially misinterpreted as ligamentous injury in four of the 46 patients (9%), all of them asymptomatic, and led to unnecessary treatment.
Following Billmann et al (13), we used a threshold value of 1.0 mm for LADI asymmetry. The incidence was lower in our posttraumatic study sample (9%) than in a different posttraumatic sample (29%) (13) and a healthy Chinese sample (31%) (20).
Unilateral alar ligament injuries seem to be rare, which aligns with our study findings (two patients [4%]). Although a biomechanical study even argues against an involvement of alar ligaments in whiplash injuries (21), Unal et al (22) suspected these injuries to be more common than diagnosed in a recent small study with only six patients.
Neck pain aggravated with rotation and dens lateralization at CT are the most significant findings for alar ligament injuries during clinical and radiologic examination (22). The discrepancy between clinical symptoms and morphologic diagnosis is a challenge in evaluating trauma patients: Patients with severe clinical symptoms may not show any cervical injuries (23,24). In addition, healthy individuals serving as control participants show signal intensity alterations and anatomic variations of alar ligaments (25–27). Chen et al (28) underlined the difficulty of differentiating between signal intensity changes due to physiologic evolution and chronic physical damage in older patients. Because it is impossible to differentiate between injuries and normal variants, Muhle et al (29) proposed that ligament injuries should be diagnosed only if tears or avulsion fractures are visible. Vetti et al (25) even concluded that additional posttraumatic cervical MRI should not be recommended because of a lack of clinical consequence. Small amounts of fluid are evident in 8% of the joints of the craniocervical junction and in 56% in the C1/C2 joints; thus, they should not be overinterpreted regarding potential CSI (30). Review of these studies illustrates that even in the acute trauma setting, differentiation between traumatic and nontraumatic ligament signal intensity changes is nearly impossible, especially if secondary signs of injury, such as hemorrhage, are missing. Therefore, we did not interpret sole ligament signal intensity alterations or adjacent asymmetric fluid collections as injuries. In that aspect, our results differ from those of other studies with a higher incidence of detected CSI at MRI. In a recent study, 92.6% of 149 “positive MRI” results were classified as “stable injuries” and consisted mainly of ligament signal intensity changes (14).
Several investigators have postulated that head rotation (13,31) and even lateral head tilt (32) result in LADI asymmetry. We found no correlation of LADI asymmetry to either of these, supporting the theory that LADI asymmetries are mostly normal variants regardless of head positioning. Nevertheless, the missing correlation between LADI asymmetry and head rotation could also be explained by the low individual head rotation (median rotation, 2.3°) in our study sample, perhaps due to the emphasis on correct head positioning in our institution.
The patient with complete rupture of the right alar ligament underwent surgery because of atlantoaxial instability, whereas the patient with partial rupture of the right alar ligament received conservative treatment with a cervical collar for 6 weeks. Four of 13 (31%) asymptomatic patients with signal intensity alterations of alar ligaments received conservative treatment with a cervical collar for 6 weeks. These treatments followed initial radiologic misinterpretation of the ligamental signal intensity alterations as injuries. Because these signal intensity alterations—according to the above-mentioned studies—should primarily not be interpreted as injuries, overtreatments have probably taken place. The use of cervical collars carries the rare risk of complications, such as pressure ulcers (19). Thus, overtreatment should be avoided. Early mobilization of the cervical spine may even be considered beneficial in stable injuries compared with continued immobilization (33,34).
The reliability and benefits of MRI in excluding alar ligament injuries are disputable. With use of intraoperative correlation, Dyas et al (35) revealed that MRI is imperfect in depicting upper cervical ligament injuries in patients with atlanto-occipital dissociation due to inconsistent and unsatisfactory inter- and intraobserver reliability. They concluded that standardized algorithms are needed for the use of MRI and interpretation of MRI findings. Moreover, additional MRI might increase the number of low-value diagnoses, risks unnecessary treatment plans, puts patients with multiple injuries at risk by necessitating a move to the MRI suite, and, at best, results in the same clinical action of collar removal (19). Some authors conclude that additional MRI after CSCT may have utility only in certain patients with persistent abnormal findings at neurologic examination (14–16,18). Our results also indicate that MRI may be beneficial only in symptomatic patients with LADI asymmetry.
Our study had limitations. Because of the retrospective design, we could not determine why some patients with LADI asymmetry and persisting symptoms were not admitted for subsequent MRI. Most patients in our study sample (36 of 46 [78%]) were asymptomatic at the cervical spine, lowering the probability for CSI. However, by strictly applying the National Emergency X-Radiography Utilization Study Group criteria and/or the Canadian C-Spine Rule, all of these patients required further CSCT, mostly because of intense trauma mechanism or other “distracting injuries” independent of the cervical spine. Moreover, the final number of patients included in our study is low. At the same time, the ratio between “true-positive” and “false-positive” cases is very low. This is most likely related to the particular scenario evaluated; mere ligamentous injuries of the upper cervical joints without concomitant fractures in general are rare. In addition, according to the Injury Severity Score and Abbreviated Injury Scale, our study sample consisted of only a few patients with serious injuries.
In conclusion, our results indicate that additional MRI for exclusion of ligamentous injuries in trauma patients with lateral atlantodental interval asymmetry may be considered reasonable only in symptomatic patients. The additional diagnostic value in clinically asymptomatic patients without proven cervical injuries seems low and may contribute to overtreatment. Larger study samples and prospective study designs are needed to eventually verify our results.
Author Contributions
Author contributions: Guarantors of integrity of entire study, C.H.E., D.G., J.A.L.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; agrees to ensure any questions related to the work are appropriately resolved, all authors; literature research, C.H.E., D.G., N.M., D.K., U.I.A., J.A.L.; clinical studies, C.H.E., D.G., A.I., N.M., D.K., C.C.P., P.A.K., J.A.L.; experimental studies, A.F., N.M.; statistical analysis, C.H.E., D.G., A.F., N.M., J.A.L.; and manuscript editing, all authors
* C.H.E. and D.G. contributed equally to this work.
A.F. supported by the BONFOR program (grant 2020-2A-04) of the Medical Faculty of the University of Bonn.
References
- 1. . Cervical spine clearance in obtunded patients after blunt traumatic injury: a systematic review. Ann Intern Med 2015;162(6):429–437.
- 2. . Assessing incidence and risk factors of cervical spine injury in blunt trauma patients using the National Trauma Data Bank. Am Surg. 2015;81(9):879–883.
- 3. . Cervical spine clearance when unable to be cleared clinically: a pooled analysis of combined computed tomography and magnetic resonance imaging. Am J Surg 2016;211(1):115–121.
- 4. . The Canadian C-spine rule versus the NEXUS low-risk criteria in patients with trauma. N Engl J Med 2003;349(26):2510–2518.
- 5.
Expert Panel on Neurological Imaging and Musculoskeletal Imaging ; Beckmann NM, West OC, . ACR Appropriateness Criteria® suspected spine trauma. J Am Coll Radiol 2019;16(5S):S264–S285. - 6. . Practice management guidelines for identification of cervical spine injuries following trauma: update from the eastern association for the surgery of trauma practice management guidelines committee. J Trauma 2009;67(3):651–659.
- 7.
ATLS Subcommittee ; American College of Surgeons’ Committee on Trauma; International ATLS working group. Advanced trauma life support (ATLS®): the ninth edition. J Trauma Acute Care Surg 2013;74(5):1363–1366. - 8. . Computed tomography versus plain radiography to screen for cervical spine injury: a meta-analysis. J Trauma 2005;58(5):902–905.
- 9. . Traumatic lesions of the occipitoatlantoaxial complex. Clin Orthop Relat Res 1989;(239):53–68.
- 10. . Spinal trauma in children. Pediatr Radiol 2001;31(10):677–700.
- 11. . Pediatric cervical spine: normal anatomy, variants, and trauma. RadioGraphics 2003;23(3):539–560.
- 12. . Asymmetry of the odontoid lateral mass interval in pediatric trauma CT: do we need to investigate further?. AJNR Am J Neuroradiol 2016;37(1):176–179.
- 13. . Occurrence and significance of odontoid lateral mass interspace asymmetry in trauma patients. World J Surg 2013;37(8):1988–1995.
- 14. . Utility of MRI for cervical spine clearance in blunt trauma patients after a negative CT. Eur Radiol 2018;28(7):2823–2829.
- 15. . Impact of MRI on changing management of the cervical spine in blunt trauma patients with a ‘negative’ CT scan. Trauma Surg Acute Care Open 2016;1(1):e00001.[Published correction appears in Trauma Surg Acute Care Open 2016;1(1):tsaco-2016-000016corr1.].
- 16. . A systematic review of the need for MRI for the clearance of cervical spine injury in obtunded blunt trauma patients after normal cervical spine CT. J Emerg Trauma Shock 2014;7(4):251–255.
- 17. . Clinical relevance of magnetic resonance imaging in cervical spine clearance: a prospective study. JAMA Surg 2014;149(9):934–939.
- 18. . The current role of magnetic resonance imaging for diagnosing cervical spine injury in blunt trauma patients with negative computed tomography scan. Am Surg 2012;78(10):1156–1160.
- 19. . Cervical spine collar clearance in the obtunded adult blunt trauma patient: a systematic review and practice management guideline from the Eastern Association for the Surgery of Trauma. J Trauma Acute Care Surg 2015;78(2):430–441.
- 20. . A three-dimensional study of the atlantodental interval in a normal Chinese population using reformatted computed tomography. Surg Radiol Anat 2011;33(9):801–806.
- 21. . Mystery of alar ligament rupture: value of MRI in whiplash injuries--biomechanical, anatomical and clinical studies [in German]. Rofo 2007;179(11):1127–113.[Published correction appears in Rofo 2007;179(12):1242.].
- 22. . Unilateral alar ligament injury: diagnostic, clinical, and biomechanical features. World Neurosurg 2019;132:e878–e884.
- 23. . Fact or fiction? MRI of alar ligaments and craniocervical junction joints in whiplash syndrome. Clin Neuroradiol 2007;17(4):215–222.
- 24. . Diagnostik und Therapie bei Beschleunigungsverletzungen der Halswirbelsäule. Dtsch Arztebl 1998;95(4):A152–A155.
- 25. . Follow-up MR imaging of the alar and transverse ligaments after whiplash injury: a prospective controlled study. AJNR Am J Neuroradiol 2011;32(10):1836–1841.
- 26. . Variability of morphology and signal intensity of alar ligaments in healthy volunteers using MR imaging. AJNR Am J Neuroradiol 2011;32(1):125–130.
- 27. . Effect of magnetic resonance imaging field strength on delineation and signal intensity of alar ligaments in healthy volunteers. Spine (Phila Pa 1976)2012;37(17):E1062–E1067.
- 28. . MR investigation in evaluation of chronic whiplash alar ligament injury in elderly patients. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2015;40(1):67–71.
- 29. . Alar ligaments: radiological aspects in the diagnosis of patients with whiplash injuries [in German]. Rofo 2002;174(4):416–422.
- 30. . MR morphology of alar ligaments and occipitoatlantoaxial joints: study in 50 asymptomatic subjects. Radiology 2001;218(1):133–137.
- 31. . Radiographic appearance of the odontoid lateral mass interspace in the occipitoatlantoaxial complex. Spine (Phila Pa 1976)1995;20(20):2221–2225.
- 32. . It is the lateral head tilt, not head rotation, causing an asymmetry of the odontoid-lateral mass interspace. Eur J Trauma Emerg Surg 2016;42(6):749–754.
- 33. . Comparison of the relative benefits of 2 versus 10 days of soft collar cervical immobilization after acute whiplash injury. Arch Phys Med Rehabil 2006;87(11):1423–1427.
- 34. . Grade II whiplash injuries to the neck: what is the benefit for patients treated by different physical therapy modalities?. Patient Saf Surg 2009;3(1):2.
- 35. . Ability of magnetic resonance imaging to accurately determine alar ligament integrity in patients with atlanto-occipital injuries. J Craniovertebr Junction Spine 2018;9(4):241–245.
Article History
Received: Nov 02 2020Revision requested: Dec 30 2020
Revision received: Mar 24 2021
Accepted: May 11 2021
Published online: June 29 2021
Published in print: Sept 2021