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Published online before print October 5, 2001, 10.1148/radiol.2212010336
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(Radiology. 2001;221:340-346.)
© RSNA, 2001


Emergency Radiology

Cervical Spine: Postmortem Assessment of Accident Injuries—Comparison of Radiographic, MR Imaging, Anatomic, and Pathologic Findings1

Axel Stäbler, MD, Jurik Eck, MD, Randolph Penning, MD, Stefan P. Milz, MD, Reiner Bartl, MD, Donald Resnick, MD and Maximilian Reiser, MD

1 From the Department of Clinical Radiology (A.S., J.E., M.R.) and Clinic of Internal Medicine III (R.B.), University Hospital Ludwig-Maximilians-University Munich, Grosshadern, Marchioninistrasse 15, 81377 Munich, Germany; Institute of Legal Medicine (R.P.) and Institute of Anatomy (S.P.M.), Ludwig-Maximilians-University Munich, Germany; and Department of Radiology, Veterans Administration Medical Center, San Diego, Calif (D.R.). Received January 24, 2001; revision requested February 21; revision received May 7; accepted May 21. Address correspondence to A.S. (e-mail: axel.staebler@ikra.med.uni-muenchen.de).


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To assess the ability of postmortem radiography and magnetic resonance (MR) imaging to depict occult cervical spine injuries as compared with anatomic and pathologic findings.

MATERIALS AND METHODS: The cervical spines of 10 adult accident victims underwent radiography and MR imaging, with T1-weighted, fast spin-echo T2-weighted, and four gradient-echo pulse sequences. The frozen specimens were cut into 3-mm-thick slices (sagittal plane) and photographed, and microfocus radiographs were obtained. Imaging findings were compared with the anatomic and pathologic findings.

RESULTS: Eight of the 10 specimens had 28 posttraumatic lesions: three fractures (two missed at the initial MR imaging reading), 10 facet joint capsule lesions with bleeding, five soft-tissue and ligament lesions, eight disk lesions, and two spinal cord lesions. Radiography depicted one lesion (4%). Two partial ruptures of the anterior annulus fibrosus were depicted at only MR imaging. Initially, 11 of 28 lesions were detected on MR images; retrospectively, 17 of 28 lesions were correlated with anatomic findings.

CONCLUSION: Soft-tissue and intervertebral disk and ligament injuries account for 89% (25 of 28) of posttraumatic cervical spine lesions detected on postmortem images. Occult lesions, including apophyseal joint injuries, were found in clinically noninjured cervical spines. MR imaging was limited in the depiction of discrete lesions when T1-weighted non–fat-saturated, fast spin-echo T2-weighted, and gradient-echo pulse sequences were used.

Index terms: Magnetic resonance (MR), comparative studies, 31.121411, 31.121412 • Spinal cord, injuries, 341.41, 341.42, 341.43 • Spine, injuries, 31.41, 34.42, 34.43 • Spine, radiography, 31.11 • Trauma, 31.40


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In acceleration or deceleration injuries, the cervical spine, with its wide range of motion and its relative lack of supporting structures, is a particularly susceptible site for injury. Injuries of the cervical spine include lesions of the bone, ligaments, and soft tissue (1,2). On the basis of the report of Jónsson et al (3), occult injuries of the cervical spine occur after trauma. Our correlation study of explanted specimens of cervical spines from accident victims without evidence of cervical spine injury included magnetic resonance (MR) imaging in the diagnostic protocol for posttraumatic lesions in cadavers. The purpose of our study was to assess the ability of postmortem radiography and MR imaging, in comparison with anatomic and pathologic findings, to depict occult cervical spine injuries.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The cervical spine from C1 or C3 to C5 or C6 (C7 in one case) was carefully removed from the cadavers of 10 consecutive accident victims (nine men, one woman; age range, 19–67 years; mean age, 39.5 years) with craniocerebral injuries that were admitted for autopsy to the Institute of Legal Medicine (Ludwig-Maximilians-University Munich, Munich, Germany). The skull base was left intact. The extent of removal of cervical spine segments depended on the anatomy and the need to restore the outer aspect of the neck. This resulted in removal of 51 vertebra with 35 intervertebral segments. Although clinical examination of the cadavers revealed that none had obvious cervical spine injuries, there was a high probability for such an injury owing to the existing head injury. The main muscles of the neck were removed, but the muscles covering the bony spine were left in place. The specimens were packed in a plastic bag and immediately frozen at -20°C. Within 2 weeks, radiography and MR imaging were performed after the specimens had thawed for 24 hours at room temperature.

Imaging
Radiographs of each specimen were obtained in the anteroposterior, lateral, and oblique projections. Screen speed was 200 (Ultra Vision; Dupont, Bad Homburg, Germany), and exposure parameters were 10 mAs and 48 keV.

MR images were obtained with a 1.5-T MR imager (Magnetom Vision; Siemens Medical Systems, Erlangen, Germany) with use of a temporomandibular joint coil. Specimens were centered in the coil and immobilized with foam pads. The imaging protocol consisted of six sequences in the sagittal plane with a section thickness of 3 mm. The field of view for all sequences was 80 x 80 mm, which resulted in an in-plane resolution of 0.31 x 0.31 mm. MR imaging was performed with the following sequences: T1-weighted spin echo (repetition time msec/echo time msec of 500/20); T2-weighted fast spin echo (4,200/17, 119); T2-weighted gradient-recalled echo fast low-angle shot, or FLASH, two-dimensional (561/15, 30° flip angle); gradient-recalled echo fast low-angle shot two-dimensional (608/15, 90° flip angle); fast low-angle shot three-dimensional fat saturated (53/11, 60° flip angle, with frequency-selective fat presaturation); and double-echo steady-state three-dimensional (26.8/9, 40° flip angle). In a preliminary study for sequence optimization, the short inversion time inversion-recovery, or STIR, sequence was removed from the imaging protocol because of an insufficient signal-to-noise ratio.

After imaging, the specimens were deep frozen at -80°C. Then, each specimen was cut into 3-mm-thick slices along the sagittal plane, and all the slices were photographed. A contact radiograph of each slice was obtained with a microfocus tube and screenless film (Faxitron; Hewlett-Packard, Palo Alto, Calif).

Some of the lesions were selected for histopathologic examination. After being embedded in methacrylate, the undecalcified specimens were sectioned (3 µm thick), and Giemsa staining was performed. For evaluation, a low-power magnification (x10) was used.

Evaluation
Only completely intact vertebrae with undestroyed intervertebral disks on both sides and completely intact intervertebral segments were evaluated. Because the field of view was restricted to 80 mm, only three to four segments of the middle and lower cervical spine were available for evaluation. Thirty-one images of intact intervertebral segments were correlated with anatomic sections.

All radiographs, MR images, and microfocus radiographs were evaluated by two observers (A.S., J.E.), who were experienced in musculoskeletal imaging. During the same session, the consensus readings started with the radiographs, followed by the microfocus radiographs. Criteria for evaluation were cortical disruption for fractures, widening of the intervertebral disk space, and intervertebral joint or spinous process distance for diskoligamentous injuries. For evaluation of the anatomic sections, which was performed later, the readers were blinded to the pathologic findings.

The MR imaging evaluation was performed 4 weeks later by the same two observers in consensus. The anterior and posterior longitudinal ligaments were evaluated for continuity and increased signal intensity on T1-weighted, T2-weighted, and gradient-recalled echo MR images. The intervertebral disks were reviewed for increased signal intensity on T2-weighted MR images and signal intensity changes on gradient-recalled echo MR images, as indicators for bleeding. The bone structures were evaluated for cortical disruption as an indication of fracture and for signal intensity increase on T2-weighted MR images in the bone marrow as an indirect sign of bone lesions. The intervertebral joints and surrounding soft tissues on T2-weighted MR images were also examined for fluid accumulations.

For pathologic evaluation, the photographs of the slices were magnified and studied by an expert in forensic medicine (R.P.). He performed a careful review of all anatomic structures, with special focus on hemorrhage in the prevertebral muscles; rupture or bleeding of the anterior or posterior longitudinal ligaments; rupture or bleeding of the anterior or posterior annulus fibrosus or nucleus pulposus; bleeding into the uncovertebral and facet joints; and bleeding into the posterior muscles, ligamenta flava, ligamenta interspinosa, and ligamentum supraspinale. The spinal canal and spinal cord were also evaluated for bleeding.

After the pathologic evaluation, a slice-by-slice comparison with direct correlation of the anatomic findings in the slices with the findings on the MR images was performed by the three readers (A.S., J.E., R.P.).


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The pathologic, radiographic, and MR imaging findings, including fractures and soft-tissue injuries, are listed in the Table. Twenty-eight posttraumatic lesions were found in eight of the 10 cervical spines.


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Postmortem Anatomic, Radiologic, and MR Imaging Findings in Noninjured Cervical Spines

 
Three (11%) of the 28 lesions were fractures. Two of the three fractures were not seen on the radiographs of the whole specimen but were detected on the contact radiographs. Radiography depicted only one of the 28 lesions. Two of the three fractures were initially missed on the MR images. Bone marrow edema of the left vertebral arch fracture of C4 in specimen 10 (Fig 1) and discrete edema in the right lamina of C5 in specimen 7 were identified retrospectively.



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Figure 1. Specimen 10, from a 30-year-old man who died after being rolled over by a train, was sectioned in the sagittal plane through the left intervertebral joints. A, Microfocus radiograph shows a fracture (arrow) of the vertebral arch of C4. B, Pathologic slice displays bleeding (arrows) in this area. C, T2-weighted MR image (4,200/17, 119) shows the edema (arrow) and fracture of the vertebral arch of C4 that was overlooked initially and recognized only retrospectively.

 
Two partial ruptures of the anterior annulus fibrosus near the anterior upper end plates of C4 and C5 were not identified in specimen 3; they were recognized only after correlation with the MR imaging findings (Fig 2). These were the only lesions that were not recognized at pathologic evaluation of the specimens.



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Figure 2. Specimen 3, from a 19-year-old man who died in an automobile accident, was obtained through the midline. A, Lateral radiograph was normal. B, Microfocus radiograph of the middle slice shows a faint radiolucency (arrow) in the anterior annulus fibrosus at the C4-5 segment near the upper end plate of C5. The radiolucency was depicted at initial radiography but was not printed clearly on the hard copy. C, Pathologic slice shows a circumscribed defect at this location (bottom arrow) and also in this area at level C3-4 (top arrow). These lesions, which showed no bleeding, were overlooked on the initial radiographs and were recognized only in comparison with the MR images. D, T2-weighted MR image (4,200/17, 119) depicts the defects of the anterior annulus fibrosus clearly at levels C3-4 (top arrow) and C4-5 (bottom arrow).

 
Only 11 of the 28 lesions were detected on the MR images during the initial blinded reading session. Seventeen of the 28 lesions were detected on MR images after direct correlation with the lesions confirmed at pathologic examination. Four cases of bleeding in the intervertebral joint and two fractures of the vertebral arch were missed in the initial reading (Figs 1, 3). These lesions were correlated retrospectively. Nevertheless, MR images were negative for 11 of the 28 lesions found at pathologic examination, even when the exact location of the bleeding was known (Fig 4).



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Figure 3. Specimen 7, from a 67-year-old man who was killed by a train, was obtained through the right intervertebral joints. A, Microfocus radiograph shows a fracture (arrow) of the right lamina of C5. B, Pathologic slice reveals bleeding (arrows) into the intervertebral joints C3-4, C5-6, and C6-7 (shown only in part, at the inferior border of the image, and not included in the Table), with avulsion of the joint capsules (arrowheads) at the posterior aspect of the inferior articular process of C3, C4, and C5 with bleeding into the soft tissue. C, T1-weighted (500/20) and D, T2-weighted (4200/17, 119) MR images depict fluid (top arrows) in the intervertebral joint C3-4 and in the soft tissue (bottom arrow) posterior to the inferior articular process of C4-5. The bleeding posterior to the inferior articular process of C3 was missed on the MR images. On the T1-weighted images, the high signal intensity of this bleeding was most probably caused by methemoglobin. E, Photomicrograph of the right intervertebral joint of C5-6 demonstrates avulsion (arrows) of the joint capsule from the posterior aspect of the inferior articular process of C5. (Giemsa stain; original magnification, x10.)

 


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Figure 4. Specimen 10, from the same patient as in Figure 1. A, Radiograph and B, microfocus radiograph were normal. C, Pathologic slice demonstrates bleeding into the anterior superior part of the annulus fibrosus (short arrow) and into the posterior nucleus pulposus (long arrow) of the C3-4 disk. D, T1-weighted (500/20), E, T2-weighted (4,200/17, 119), and F, gradient-recalled echo (608/15 with 90° flip angle) MR images were interpreted as normal.

 
Diskoligamentous disruption after a hyperextension injury was present in one specimen. Avulsion of the anterior longitudinal ligament and disk disruption were complete, while the posterior longitudinal ligament was only stretched (Fig 5). The pathologic findings correlated with the MR imaging findings.



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Figure 5. Specimen 7, from the same patient as in Figure 3. A, Lateral radiograph shows a tear drop fracture (arrow) at the lower anterior aspect of C3, with normal alignment. B, Microfocus radiograph shows the fracture (arrow) more clearly. C, Pathologic slice displays bleeding (arrow) into the disk space of C3-4, which indicates a disk injury. D, T1-weighted (500/20) and E, T2-weighted fast spin-echo (4,200/17, 119) MR images show a diskoligamentous hyperextension injury with avulsion of the anterior longitudinal ligament (long arrow in E) from the anterior cortex of C3, the tear drop fracture (short arrow in E), and the disk lesion (arrowhead in E) and partial rupture (arrow in D) of the posterior longitudinal ligament, with increased signal intensity in D. F, Photomicrograph displays the avulsion of the anterior longitudinal ligament (arrows), displaced tear drop fracture, disk disruption, and incomplete lesion of the posterior longitudinal ligament (curved arrow). (Giemsa stain; original magnification, x10.)

 
MR images tended to depict lesions of the disk, annulus fibrosus, and anterior longitudinal ligament better than lesions of the apophyseal joints and soft tissue. Lesions of the facet joints were detected only indirectly on the basis of depiction of fluid in the joint. Direct depiction of the ruptured apophyseal joint capsule was almost impossible (Fig 3). If lesions of the disk and diskovertebral junction were depicted, their nature could be determined (Figs 2, 5).


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The cervical spine is susceptible to injuries during hyperextension or hyperflexion. These injuries have been described previously (1,47). Only 20% of cervical spine injuries are represented by a fracture; even in fatal cases, 80% of traumatic lesions are injuries of the soft tissues (8). Before the availability of MR imaging and computed tomography, radiography and clinical examinations were the only methods for investigating cervical spine injuries. In 22 traffic accident victims with skull fractures, Jónsson et al (3) found 245 bone, diskoligamentous, and soft-tissue lesions of the cervical spine that were not detected on radiographs. In addition, Webb et al (9) reported the cases of seven patients with hidden flexion injuries of the cervical spine that were not detected on radiographs.

Findings in our comparison study confirmed these results. Twenty-five (89%) of 28 lesions detected during the study were injuries to soft-tissue structures, including the longitudinal ligaments, the disks, and the apophyseal joint capsules. Only three of the 28 lesions were fractures; two were missed on the radiographs. These findings are consistent with results in the studies by Jónsson et al (3) and Saternus (8), who found that fractures contributed to 20.0%–22.7% of the injuries overall (3,8).

Hyperextension injuries of the cervical spine are common and are associated with a risk of spinal cord compromise of variable degree even in the presence of normal radiographs (1013). Degenerated segments with fissuring of the disk expose the longitudinal ligament to increased loading forces and increased risk of hyperextension injury (10,14). The spectrum of cervical hyperextension injuries ranges from muscle sprains to serious lesions, such as diskoligamentous disruption (12). In hyperextension injuries, both the anterior and posterior longitudinal ligaments are stretched or disrupted, the anterior longitudinal ligament more severely, which causes hemorrhage beneath the prevertebral fascia and occasional avulsion fragments from the anterior margin of the vertebra (12). Diagnosis of hyperextension injuries may be difficult because they often show only subtle radiographic abnormalities, even in severe or unstable lesions (10,15,16).

In young persons, a special form of lesion in the intervertebral segment can occur, with characteristic separation of the intervertebral disk from the vertebral end plate (2,17,18). After a severe neck injury, complete horizontal rupture of a disk was not observed in the presence of an intact nucleus pulposus (8). The annulus fibrosus itself can remain intact in a hyperextension injury, and a partial or complete avulsion of the fibro-osseous junction, including the hyaline cartilage end plate, can occur at the ossified ring apophysis. In the cadaver of a 19-year-old accident victim, we documented the imaging appearance of an incomplete avulsion of the anterior annulus fibrosus, with water signal intensity in the defect (Fig 2). These two lesions were not identified at the initial evaluations of the anatomic sections owing to the lack of bleeding. A similar injury was documented by Davis et al (12) at MR imaging in a patient. Incomplete lesions of the annulus fibrosus may also occur in whiplash injuries.

Incomplete avulsion of the anterior annulus fibrosus is responsible for the vacuum phenomenon observed by Reymond et al (19), Resnick et al (20), and Bohrer (21). This vacuum cleft might be called an annulus cleft to differentiate it from a nucleus cleft, which occurs in the center of the disk (16,22). This annulus cleft vacuum phenomenon after hyperextension injury of the cervical spine is located in the anterior portion of the annulus fibrosus and not in the center of the nucleus pulposus. The high amount of water inside an intact nucleus pulposus makes the occurrence of a vacuum unlikely. In our study, an anterior vacuum phenomenon depicted on lateral MR images of the cervical spine in extension in a young patient without preexisting degenerative changes probably represents this type of partial rupture of the annulus (Fig 2). The anterior longitudinal ligament remained intact, and stability was preserved.

Hyperflexion injuries of the cervical spine can cause partial or complete disruption of the posterior cervical complex, which comprises the posterior articulations stabilized by the joint capsule, interspinous and supraspinous ligaments, and ligamenta flava (9). No clear border exists between maximal physiologic flexion and partial subluxation on lateral radiographs obtained in flexion and extension, which allows different interpretations. It is also difficult to decide whether the lesion is complete and unstable or only a partial tear without instability (9,23).

Because anterior subluxation can represent an unstable cervical spine injury, diagnosis of instability is crucial (24). Soft-tissue damage in anterior cervical subluxation may be severe, and late progressive displacement can occur with persisting instability and varying neurologic sequelae (25,26). MR imaging has proved to be more accurate than conventional radiography in the depiction of a wide spectrum of neck injuries, because it is capable of direct depiction of disruption of the joint capsule of the apophyseal joints, the ligamenta flava, and the inter- and supraspinous ligaments (4,27). In our series, the most frequently injured sites were the apophyseal joints, and the most frequently missed lesions were in the posterior elements.

The conditions of MR imaging during our study were superior to those associated with in vivo studies in several respects. First, motion artifacts were not a concern in the investigations of the specimens. Second, three acquisitions were performed with all sequences to gain a high signal-to-noise ratio for improved image quality, which resulted in an acquisition time of 6 minutes 3 seconds to 13 minutes 37 seconds. Such long acquisition times in a clinical setting may result in degradation of image quality due to motion. Finally, removal of major parts of the soft tissues of the neck enabled the use of a temporomandibular joint coil. In addition, a field of view of 80 x 80 mm, which results in an in-plane resolution of 0.31 mm, is not suitable for MR imaging investigation of the whole cervical spine, which would necessitate use of a field of view of 140 x 140 mm or greater. The signal-to-noise ratio with the head and neck surface coil is less than that with a temporomandibular joint coil.

The major limitation of our imaging protocol was the lack of a highly sensitive water sequence, such as the short inversion time inversion-recovery or T2-weighted fat-saturated sequences. As a result of the pulse arrangement, these sequences generally have a low signal-to-noise ratio. Because signal is dependent on temperature, the decreased temperature of the specimen (19°C) compared with the in vivo temperature (37°C) may account for the inferior signal-to-noise ratio.

In conclusion, this correlation study of postmortem MR imaging, conventional radiographic, microfocus radiographic, and pathologic findings of cervical spines in accident victims confirmed the high frequency of associated cervical spine injuries after severe head injuries. In our study, nearly 89% (25 of 28) of the posttraumatic lesions were soft-tissue lesions; only three of the 28 lesions were fractures, and only one was visible on the radiographs.

An incomplete hyperextension injury with incomplete rupture of the anterior annulus fibrosus was depicted at MR imaging. We presumed that this type of injury was responsible for a vacuum phenomenon (annulus cleft), which can be seen occasionally on lateral images of the cervical spine in extension obtained after acceleration injuries of the cervical spine.

Findings in our study showed the limitations of MR imaging for depicting posttraumatic lesions of the lower cervical spine with gradient-recalled echo, T1-weighted, and non–fat-saturated fast spin-echo T2-weighted sequences. Inversion-recovery sequences with a short inversion time or fat-saturated T2-weighted sequences might be more effective for depicting many of the soft-tissue injuries in patients. Our study involved direct comparison of posttraumatic cervical spine lesions with imaging findings. Various occult lesions, including many apophyseal joint injuries, which can also occur in survivors of vehicle accidents, were found on postmortem MR images obtained in clinically noninjured cervical spines.


    FOOTNOTES
 
Author contributions: Guarantor of integrity of entire study, A.S.; study concepts and design, A.S., D.R.; literature research, J.E., A.S.; experimental studies, J.E., A.S., R.P., S.P.M., R.B.; data acquisition, J.E., A.S., R.P., S.P.M.; data analysis/interpretation, R.B., A.S., R.P., J.E.; manuscript preparation, A.S., M.R.; manuscript definition of intellectual content, A.S.; manuscript editing, A.S., M.R., D.R.; manuscript revision/review, M.R., D.R.; manuscript final version approval, A.S.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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