MRI of the tectorial and posterior atlanto-occipital membranes in the late stage of whiplash injury

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1 Neuroradiology (2003) 45: DOI /s DIAGNOSTIC NEURORADIOLOGY J. Krakenes B. R. Kaale G. Moen H. Nordli N. E. Gilhus J. Rorvik MRI of the tectorial and posterior atlanto-occipital membranes in the late stage of whiplash injury Received: 31 March 2003 Accepted: 22 April 2003 Published online: 5 August 2003 Ó Springer-Verlag 2003 J. Krakenes (&) Æ G. Moen Æ H. Nordli J. Rorvik Department of Radiology, University of Bergen and Haukeland University Hospital, 5021 Bergen, Norway jostein.krakenes@helse-bergen.no Tel.: Fax: B. R. Kaale Firda Medical Centre, 6823 Sandane, Norway N. E. Gilhus Department of Neurology, University of Bergen and Haukeland University Hospital, 5021 Bergen, Norway Abstract Our aim was to characterise and classify permanent structural changes in the tectorial and posterior atlanto-occipital membranes several years after a whiplash injury, and to evaluate the reliability of our classification. We obtained sagittal proton density-weighted images of the craniovertebral junction of 92 whiplash-injured and 30 uninjured individuals. Structural abnormalities in the two membranes were classified as grades 1 3 independently by three radiologists blinded for clinical information. Grading criteria were based on reduced tectorial membrane thickness, and elongation or rupture of the posterior atlanto-occipital membrane/dura mater complex. The same images were reassessed 4 months later. Image quality was graded good in 104 cases, slightly reduced in 13 and unsatisfactory in five. Of 117 tectorial membranes 31 (26.5%) showed grade 2 or 3 lesions, in the uninjured group none were grade 3 and only three were grade 2. Pair-wise interobserver agreement (weighted kappa) was moderate ( ), while the intraobserver agreement was moderate to good ( ). Of 117 posterior atlanto-occipital membranes 20 (17.1%) had grade 2 or 3 lesions; there was no grade 3 and only one grade 2 lesion in the uninjured group. Interand intraobserver agreement was good ( and , respectively). Reduced image quality was the main reason for disagreement, but partial thinning and lateral tapering, as normal tectorial membrane variations, created difficulties in some cases. This study strongly indicates that whiplash trauma can damage the tectorial and posterior atlanto-occipital membranes; this can be shown on highresolution MRI. Better knowledge of normal anatomical variations and improved image quality should lincrease the reliability of lesion classification. Keywords Cervical spine Æ Craniovertebral junction Æ Tectorial membrane Æ Posterior atlanto-occipital membrane Æ Whiplash injury Æ Magnetic resonance imaging Introduction Craniovertebral stability depends on the integrity of ligamentous structures. The alar and transverse ligaments are considered the most important and have been thoroughly analysed [1, 2, 3, 4]. Less attention has focused on the tectorial and atlanto-occipital membranes. The tectorial membrane, a strong collagenous band, appears as an upward extension of the posterior longitudinal ligament of the vertebral column. It is fixed caudally to the body of C2, and cranially to the basilar groove of the occipital bone. From the dens upwards it

2 586 is indistinguishable from the dura mater. The posterior atlanto-occipital membrane, an extension of the highly elastic ligamentum flavum, runs from the posterior arch of the atlas to the posterior margin of the foramen magnum. It joins the posterior dura mater of the vertebral canal [5]. The functional significance of these membranes has been examined in a cadaver study by sequential sectioning [6]. Sectioning of the anterior or posterior atlanto-occipital membrane alone did not make the neck unstable. Incision of the tectorial membrane was accompanied by translation in flexion. When all three membranes were incised, gross instability was observed, especially in flexion. To the best of our knowledge the pathology of these membranes has never been examined in vivo. We have recently used high-resolution MRI to analyse the alar ligaments [7, 8]. In the present study, we assessed structural changes in the tectorial and atlanto-occipital membranes several years after a whiplash injury and in healthy subjects. Materials and methods All individuals diagnosed as having a recent whiplash injury by their primary-care doctor in seven rural communities in Western Norway were registered prospectively during Only patients classified as injury grade 2 after weeks were included. Grade 2 defined by the Que bec Task Force of Whiplash-associated Disorders [9] is: neck complaints and musculoskeletal signs including reduced range of neck movement and local tenderness; no neurological signs, including decreased or absent deep tendon reflexes, paresis and/or sensory deficits. Neck radiographs with Fig. 1a d Sagittal proton density (2660/15) sections of typical appearances. a Normal b d injured tectorial membranes. a Parasagittal section showing the dura mater (arrow) and the tectorial membrane (arrowhead) before they merge at the dens (double arrow). b Discontinuity of a short segment; only the dura mater is present (double arrow). Normal membrane above and below indicates a rupture (black arrows). c Absence of the entire membrane (black arrow); only the dura mater is present (double arrow). d Absence of the membrane (black arrow) and focal thinning of the dura mater (double arrow) indicating a severe injury extension and flexion views in the acute phase were normal in all. There were 342 registered patients, from which a random sample of 100 were invited to participate; 93 accepted and gave their informed consent, but one had to be excluded because of claustrophobia. Thus 33 males and 59 females, mean age 40 years (range years) underwent MRI, 2 9 years (mean 6 years) after the injury. We also studied 30 individuals with no history of head or neck trauma, from the same seven Norwegian communities and matched for age and sex, as a control group. We invited 100 individuals, of whom 75 were willing to participate, but five were excluded because of previous neck trauma. Of 50 drawn randomly from this sample of 70, 30 attended for MRI examination: 11 men, 19 women, mean age 46 years (range years). Images were obtained at 1.5 tesla, using fast spin echo protondensity-weighted sequences. We obtained 15 2 mm interleaved sagittal sections of the craniovertebral junction, covering the area from the clivus to C2, TR 2660 TE 15 ms, matrix , field of view mm and craniocaudad phase-encoding, four acquisitions, echo-train length seven and receiver bandwidth 130 Hz/pixel. We applied saturation pulses anterior, superior and inferior to the volume of interest; imaging time was 6 min 13 s. Pixel size was mm, implying that structures down to 0.5 mm could be discriminated. The cranial segment of the tectorial membrane, between the dens and the clivus, is adherent to and indistinguishable from the dura mater on sagittal images. A normal membrane/dura mater complex from the dens upwards cranially is shown as a dark band, mean thickness 1.4 mm [7] (Fig. 1a). A thinner membrane/dura mater complex, similar to the dura mater alone, was regarded as indicating a ruptured membrane; such defects could involve a short segment or the entire length of the structure (Fig. 1b d). Grading was based on the fraction of the total transverse width (number of sagittal slices) with reduced thickness (Table 1). The posterior atlanto-occipital membrane connects the posterior arch of C1 and the posterior margin of the foramen magnum. On sagittal images it appears as a dark band fused with the dura mater (Fig. 1a), or separated from the latter by a connectivetissue layer (Fig. 1b). We based our grading of the membrane/ dura mater complex on structural changes of the adjoining dura mater: a dural hump, thinning, a flap and discontinuity (Fig. 2). A dural hump or thinning was taken as elongation of the dura mater and regarded as a sign of minor sprain, whereas a dural flap or discontinuity was regarded as rupture and thus a more pronounced lesion. Grading was based on the extent of these changes (Table 1). The images of the 92 injured and 30 uninjured individuals were mixed in random order. They were reviewed twice at a 4-month interval, by the same three radiologists, blinded to all clinical information. Membranes rated two or more grades differently in the first and second sessions were reassessed, and each observer identified possible reasons for divergent rating. The same was done

3 587 Table 1 Criteria for classification of the tectorial and posterior atlanto-occipital membranes Grade Criteria Tectorial membrane 0 A membrane/dura mater complex thicker than the dura mater alone in all sagittal sections 1 Only dura mater left in <1/3 transverse width 1 2 Only dura mater left in 1/3 2/3 transverse width 3 Only dura mater left in >2/3 transverse width Posterior atlanto-occipital membrane 0 Smooth and well-defined membrane/dura mater complex 1 Thinning, minor discontinuity or a dural hump in <1/3 transverse width a 2 As grade 1 affecting 1/3 2/3 transverse width 3 Discontinuity with or without a dural flap in >2/3 transverse width a Transverse width was estimated by numbering all images in which the membranes could be appreciated Fig. 2a d Sagittal proton density sections of abnormal posterior atlanto-occipital membranes. a Dural irregularity or hump (arrowhead). b Dural thinning (arrowhead); the membrane is invisible and could be ruptured. c, d Dural rupture with c an anteriorly protruding flap (arrowhead) and d persisting discontinuity (arrowhead). The tectorial membrane is normal in all cases where all three observers disagreed in the second review. Two observers (J.K., G.M.) had 10 years of experience with MRI and H.N. 3 years. To obtain mutual understanding of the grading criteria, we carried out a pilot study of 30 cases. Interpretation and results were compared, and differences in the application of the criteria were extensively discussed. Kappa coefficients (K) were used to evaluate intraobserver agreement (comparing the first and second interpretations) and pair-wise interobserver agreement. Ordinary K were calculated on the basis of all four MRI gradings (0 3). The ordinary K puts equal weight on disagreements of one or more steps. To include the amount of disagreement, we also calculated weighted K. Differences in rating were weighted as follows: full agreement: 1; a one-step difference: 0.67; a two-step difference: 0.33; a three-step difference; To evaluate the effectiveness of our method to distinguish normal and slightly abnormal membranes (grades 0 1) from obviously injured membranes (grades 2 3), our data were dichotomised. We also calculated 95% confidence interval for the K coefficients [10]. K <0.20 is generally regarded as indicating poor, fair, moderate and >0.60 good agreement [11]. Consistent differences between the first and second gradings, and pair-wise differences between two observers, where one observer consistently reported higher or lower grades, were examined by McNemar s test for symmetry [12, 13]. Results Image quality was judged good in 104 cases, slightly reduced in 13 and unsatisfactory in five cases due to motion or cerebrospinal fluid motion artefacts. Thus the tectorial and the posterior atlanto-occipital membranes could be assessed in 117 of 122 individuals, 90 in the injured and 27 in the uninjured group. Lesions in the tectorial membrane could be unilateral (Fig. 3) or bilateral (Fig. 4). They could affect a short segment (Fig. 1b), the whole length (Fig. 1c), or even the dura mater could be thinned or partially ruptured (Fig. 1d). Grading criteria are shown in Table 1. Pair-wise interobserver calculations for the second assessment for the four tectorial membrane grades showed ordinary K consistent with fair agreement ( ), and moderate agreement ( ) with weighted K showed. Dichotomising the groups (grades 0 1 versus 2 3) did not improve agreement. Two observers (GM and HN) rated significantly higher (more membrane lesions) than the third ( P <0.05). Intraobserver ordinary K was fair to moderate ( ), and weighted K moderate to good ( ) with no further improvement by dichotomising the groups. Two observers graded significantly higher in the first than in the second session ( P <0.05) (Table 2). Full agreement or a one-step difference in the first and second gradings

4 588 Fig. 3a g Contiguous sagittal proton density sections of the tectorial membrane from right to left. a d Substantial thinning of the right half (arrows). e g Normal thickness on the left (double arrows). Between one and two thirds of the membrane is injured (grade 2) was obtained for 93.2% of the MRI studies for all three observers taken together. A two or three-step intraobserver disagreement occurred in 24 cases (3, 11 and 10 for J.K., G.M. and H.N., respectively). In the second assessment two or three observers classified 44 membranes as grade 0, 15 in the uninjured group; 25 as grade 1, six in the uninjured group; 19 as grade 2, three in the uninjured group, and 12 as grade 3, all in the whiplash group. Typical grade 3 appearances are shown in Figs. 3 and 4. In 17 membranes (14.5%), four in the uninjured group, no agreement was reached by the three observers. Reasons for disagreement were reduced image quality, partial thinning of the membrane, intermediate signal from the membrane, interpretation flaws and difficulties in discriminating between normal tapering and thinning due to a lesion. A dural hump in the posterior atlanto-occipital dura mater was usually seen in the medial portion (Fig. 2a), whereas dural thinning was often asymmetrical (Fig. 5). Dural flaps always involved the entire transverse width Fig. 4a g Contiguous sagittal proton density sections all showing a discontinuity of the tectorial membrane (black arrows), indicating a grade 3 lesion. Only the dura mater remains at the rupture site (Fig. 6). The membrane alone, was usually difficult to assess independently of the dura mater. It was usually well defined in lower grades, whereas in grades 2 3 it could show increased signal or be partially or totally absent (Figs. 5, 6). Pair-wise interobserver analysis for the second assessment of all four posterior atlanto-occipital membrane grades showed an ordinary K consistent with moderate agreement ( ), whereas weighted K showed good agreement ( ). Dichotomising the groups (grades 0 1 versus 2 3) still showed good agreement. One observer (H.N.) rated significantly higher (more membrane lesions) than the others (P <0.05). Ordinary K for the intraobserver study was moderate to good ( ), and weighted K good ( ), including when we dichotomised the groups (Table 3). Agreement or a one-step difference in the first and second gradings was obtained for 99.8% of the membranes for all three observers. A two or three-step intraobserver disagreement occurred in six cases (one, three and two for J.K., G.M. and H.N., respectively). Two or three observers classified 71 membranes as grade 0, 22 in the uninjured group; 23 as grade 1, three in the uninjured group; nine as grade 2, one in the uninjured group and 11 as grade 3, all in the whiplash group. In three cases, one in the uninjured group, no agreement was reached. Reasons for inter- and intraobserver disagreement were reduced image quality due to motion or interpretation flaws.

5 589 Table 2 Pair-wise inter- and intraobserver agreement, kappa coefficients (K) for agreement and P values (McNemar s test for symmetry) for 117 tectorial membranes graded twice (grades 0 3) by three observers (J.K., G.M., H.N.) Observers % In each grade Disagreement (%) K (95% confidence intervals) P Ordinary Weighted 2nd grading J.K. vs G.M ( ) 0.50 ( ) <0.01 a J.K. vs H.N ( ) 0.50 ( <0.01 a H.N. vs G.M ( ) 0.47 ( ) st vs 2nd grading J.K ( ) 0.70 ( ) 0.41 G.M ( ) 0.51 ( ) <0.01 b H.N ( ) 0.53 ( ) <0.01 b a G.M., H.N. significantly higher than J.K. b G.M. and H.N. significantly higher in first grading Fig. 5a g Contiguous sagittal proton density sections of a severely injured posterior atlanto-occipital membrane. a, b Normal dura mater (white arrows). c Dural thinning (arrowhead). d g Invisible dura mater (black arrows). The posterior atlanto-occipital membrane (arrowhead) is absent in all section Fig. 6a g Contiguous sagittal proton density sections showing a transverse rupture of the posterior atlanto-occipital dura mater, indicating a grade 3 lesion. A dural flap (white arrows) protrudes into the subarachnoid space. Parts of the membrane show increased signal (black arrows) Discussion We demonstrated structural abnormalities of the craniovertebral membranes and the adjacent dura mater several years after whiplash injury. The lesions, including ruptured membranes, we graded according to severity. In a random sample of whiplash injured individuals 27% had grade 2 3 lesions of the tectorial membrane and 17% of the posterior atlanto-occipital membrane. Only minor changes were found in a control

6 590 Table 3 Pair-wise inter- and intraobserver agreement, K for agreement and P (McNemar s test for symmetry) from second grading for 117 posterior atlanto-occipital membranes graded twice (grades 0 3) by three observers (J.K., G.M., H.N.) Observers % in grades Disagreement (%) K (95% confidence intervals) P Ordinary Weighted 2nd grading J.K. vs G.M ( ) 0.70 ( ) 0.08 J.K. vs H.N ( ) 0.74 ( ) 0.04 a H.N. vs G.M ( ) 0.61 ( ) <0.01 a 1st vs 2nd grading J.K ( ) 0.86 ( ) 0.79 G.M ( ) 0.72 ( ) 0.84 H.N ( ) 0.65 ( a H.N. significantly higher than J.K., G.M group, indicating that the abnormalities are caused by the only known neck injury in the study group. To our knowledge these membranes have previously not been addressed as a potential injury site after whiplash trauma. Membrane rupture has, however, been demonstrated in children sustaining severe craniovertebral injuries with atlanto-occipital dissociation [14, 15]. These structures are also vulnerable to nondislocation trauma. Examining the victims of 21 fatal traffic accidents without craniovertebral dislocation, Adams [16] found 13 dural and tectorial membrane lesions. Cervical MRI protocols with 3 5 mm thick slices are inadequate to demonstrate such membrane lesions [7]. Sections 2 mm thick gave adequate spatial resolution with fairly good signal-to-noise. The low membrane signal on proton density-weighted images gave good delineation from both cerebrospinal fluid and adjacent soft tissue. The tectorial membrane plays a substantial role in maintaining stability in the craniovertebral junction, especially by limiting flexion [6]. During whiplash trauma hyperextension, hyperflexion and translation take place in the upper cervical spine [17, 18, 19]. Hyperflexion alone or combined with anterior translation is the presumed mechanism for damage to this membrane. We saw all grades of thinning of the tectorial membrane. Partial thinning can represent a normal variant [7]. However, complete absence of the membrane, with normal or partially ruptured dura mater, was never found in the control group and we therefore regarded it as trauma-induced. In hyperflexion trauma all posterior cervical ligaments and membranes are subject to strain forces. When the atlanto-occipital membrane is stretched beyond its elastic limit, these forces are transmitted to the adjacent dura mater. Rupture of the latter therefore indicates a sprained membrane. To establish consistent criteria for assessment of the posterior atlanto-occipital membrane, it was necessary to include the adjacent dura mater. We regarded a dural hump or thinning as signs of partial membrane sprain, and dural discontinuity or a flap as indicating more severe sprain or even rupture, which could be seen as an ill-defined or invisible membrane. The reliability of MRI assessment of the tectorial membrane, as judged by K values was moderate to good. Severity grading of a disease based on diagnostic imaging typically shows greater observer variation than measurement studies or diagnosing the presence or absence of a condition [20]. The K values show that the grading criteria are applicable, although the consistency would have been better if the level of knowledge at the study outset had been better. Only a small pilot study was undertaken as training for the observers prior to the evaluation. The subtle difference between partial thinning and complete absence of a membrane is a crucial point that could be focused upon in radiology training. Partial thinning of the membrane/dura mater-complex could represent an incomplete tear or an anatomical variation. An irregular anterior margin of the tectorial membrane occurs normally, but can simulate a partial tear [7]. To diagnose a membrane lesion the dura mater should be the only remnant lining between the dens and the clivus. Another difficulty in assessing the tectorial membrane was to differentiate between a lesion and the natural tapering of the membrane towards the lateral margins. A lateral lesion should be diagnosed only when a focal discontinuity is observed or when a thinning is present on one side and not on the other. Inter- and intraobserver agreement for the posterior atlanto-occipital membrane was good for all observers. The differentiation between thinning, discontinuity and rupture was obvious for most cases. Thus, the classification of the atlanto-occipital membrane/dura matercomplex lesions did not cause major difficulties. In classifying injured ligaments and membranes there will be equivocal cases. Hence, a one-step difference in grading does not necessarily indicate real disagreement. The weighted K coefficient was used and, as expected,

7 591 considerably better values were found when degree of disagreement was taken into consideration. Dichotomising the groups did not improve intra- and interobserver agreement. Thus, a classification of these membrane lesions into four grades (0 3) seems appropriate. Acknowledgements We gratefully acknowledge Grethe Albrektsen PhD, Section of Medical Statistics, for statistical calculations and helpful suggestions; Leif Arve Abildgaard RT, Department of Radiology, for configuring the MRI sequences and Joost Gravendeel MD, Department of Radiology, for technical support with the illustrations. References 1. Dvorak J, Schneider E, Saldinger P, Rahm B (1988) Biomechanics of the craniocervical region: the alar and transverse ligaments. J Orthop Res 6: Heller JG Amrani J, Hutton WC (1993) Transverse ligament failure; a biomechanical study. J Spinal Disord 6: Saldinger P, Dvorak J, Rahn BA, Perren SM (1990) Histology of the alar and transverse ligaments. Spine 15: Dickman CA, Mamourian A, Sonntag VK, Drayer BP (1991) Magnetic resonance imaging of the transverse atlantal ligament for the evaluation of atlantoaxial instability. J Neurosurg 75: Soames RW (1995) Skeletal system. In: Gray H et al (eds) Gray s anatomy, 38th edn. Churchill Livingstone, New York, pp Harris MB, Duvla MJ, Davis JA Jr, Bernine PM (1993) Anatomical and roentgenographic features of atlantooccipital instability. J Spinal Disord 6: Krakenes J, Kaale BR, Rorvik J, Gilhus NE (2001) MRI assessment of normal ligamentous structures in the craniovertebral junction. Neuroradiology 43: Krakenes J, Kaale BR, Moen G, Nordli H, Gilhus NE, Rorvik J (2002) MRI assessment of the alar ligaments in the late stage of whiplash injury a study on structural abnormalities and observer agreement. Neuroradiology 44: Erratum: Neuroradiology 44: Spitzer WO, Skovron ML, Salmi LR, et al (1995) Scientific monograph of the Quebec Task Force on Whiplash-Associated Disorders: Redefining whiplash and its management. Spine 20: 1S 73S 10. Fleiss JL (1981) Statistical methods for rates and proportions, 2nd edn. Wiley, New York, pp Altman DG (1997) Practical statistics for medical research. Chapman & Hall/ CRC, London, pp Altman DG (1997) Practical statistics for medical research. Chapman & Hall/ CRC, London, pp Brennan P, Silman A (1992) Statistical methods for assessing observer variability in clinical measures. Br Med J 304: Grabb CB, Frye TA, Hedlund GL, Grabb PA, Royal SA (1999) MRI diagnosis of suspected atlanto-occipital dissociation in childhood. Pediatr Radiol 29: Sun PP, Poffenbarger GJ, Durham S, Zimmerman RA (2000) Spectrum of occipitoatlantoaxial injury in young children. J Neurosurg 93 [Suppl 1]: Adams VI (1993) Neck injuries: III. Ligamentous injuries of the craniocervical articulation without occipito-atlantal or atlanto-axial facet dislocation. A pathologic study of 21 traffic fatalities. J Forensic Sci 38: Grauer JN, Panjabi MM, Cholewicki J, Nibu K, Dvorak J (1997) Whiplash produces an S-shaped curvature of the neck with hyperextension at lower levels. Spine 22: Grifka J, Hedtmann A, Pape HG, Witte H, Bar HF (1998) Biomechanics of injury of the cervical spine Orthopa de [German] 27: Penning L (1998) Backward hypertranslation of the head: participation in the whiplash injury mechanism of the cervical spine? Orthopa de [German] 23: Robinson PJ (1997) Radiology s Achilles heel: error and variation in the interpretation of the Ro ntgen image. Br J Radiol 70: