Abstract
Study Design:
Retrospective cohort study.
Objective:
To develop a grading method for cervical paraspinal soft tissue damage after cervical spinal cord injury (CSCI) without major fracture based on the short T1 inversion recovery (STIR) mid-sagittal magnetic resonance image (MRI) for prediction of neurological improvements.
Methods:
This study included 34 patients with CSCI without major fracture, treated conservatively for at least 1 year and graded using the STIR-MRI Grade. This system consists of anterior grades; A0: no high-intensity area (HIA), A1: linear HIA, and A2: fusiform HIA, and posterior grades; P0: no HIA, P1: HIA not exceeding the nuchal ligament, and P2: HIA exceeding the nuchal ligament, within 24 hours postinjury. The American Spinal Injury Association impairment scale (AIS) and the Japanese Orthopedic Association (JOA) scores were examined.
Results:
Anterior grades were not significantly correlated with the AIS and JOA score. At both injury and final follow-up, the AIS in P2 patients was significantly more severe (P = 0.007, P = 0.015, respectively) than that in P0 patients. At the injury, the AIS in P2 patients was significantly more severe (P = 0.008) than that in P1 patients. Among P2 patients only, the JOA score at the injury (1.4 points) did not improve by the final follow-up (3.9 points). The final follow-up JOA score (3.9 points) in P2 patients was significantly lower than that (13.6 points) in P0 patients (P = 0.016).
Conclusions:
Grade P2 led to poor neurological outcomes. The STIR-MRI Grade is a prognostic indicator for neurological improvements past-CSCI.
Keywords: cervical spinal cord injury, grading, STIR, paraspinal soft tissue, neurological outcome
Introduction
There have been several reports on the relationship between paraspinal soft tissue damage observed on magnetic resonance images (MRI) for cervical spinal cord injury (CSCI) without major fracture and the clinical relevance.1-3 These reports evaluated the high-intensity area (HIA) of the anterior paraspinal soft tissue using T2-weighted MRI. However, there have been no reports regarding the relationships between the signal change of the posterior paraspinal soft tissue on MRI and the neurological outcomes after CSCI.
While T2-weighted MRI shows HIA not only in oedema with bleeding but also in fat tissue, the short T1 inversion recovery (STIR) MRI is helpful in the diagnosis of soft tissue and ligamentous injuries because STIR images are highly sensitive for the detection of edema. 4 The authors have also frequently encountered patients with signal changes in posterior paraspinal soft tissue on STIR MRI after CSCI despite no major fractures. The authors speculated that signal changes in the posterior paraspinal soft tissue on STIR MRI might express the severity of the injury more clearly than T1 or T2-weighted MRI. However, the relationship between posterior paraspinal soft tissue damage on STIR MRI and neurological outcomes remains unclear, with no reports to our knowledge in the literature.
This study aimed to define a new grading system for cervical paraspinal soft tissue damage based on STIR mid-sagittal MRI, referred to as the “STIR-MRI Grade”, in patients with CSCI without major fracture. Additionally, we aimed to clarify whether the STIR-MRI Grade is related to neurological improvements after CSCI.
Materials and Methods
Study Population
Thirty-four patients (21 men) who had had CSCI without major fracture were included in this study. All patients underwent STIR mid-sagittal MRI within 24 hours after injury, and all patients were treated conservatively for more than 1 year after injury. A small avulsion fracture of the vertebral body, a spinous process fracture, or a bone bruise in the vertebral body without noticeable vertebral collapse was considered a minor bony injury, and these injuries were included in this study.
Grading of Paraspinal Soft Tissue Damage Using the STIR-MRI Grade
The high-intensity of the anterior or posterior paraspinal soft tissue area was qualitatively evaluated using STIR mid-sagittal MRI, i.e., STIR-MRI Grade, within 24 hours after injury. Anterior grades (Figure 1) and posterior grades (Figure 2) were classified into three grades, as shown in Table 1. The injury level was defined by neurological examination and the existence of intramedullary high-intensity on T2-weighted mid-sagittal MRI.
Figure 1.
Anterior grades were classified into three grades based on the shape of the high-intensity area in the prevertebral area using the STIR-MRI Grade. A0: no high-intensity area (a); A1: linear high-intensity area (dotted circle) (b); A2: fusiform high-intensity area (dotted circle) (c).
Figure 2.
Posterior grades were classified into three grades based on the extent of the high-intensity area in the posterior paraspinal soft tissue using the STIR-MRI Grade. P0: no high-intensity area (a); P1: high-intensity area (dotted circle) not exceeding the nuchal ligament (arrows) (b); P2: high-intensity area (dotted circle) exceeding the nuchal ligament (arrows) (c).
Table 1.
The STIR-MRI Grades for Evaluation of Paraspinal Soft Tissue Damages After CSCI without Major Fracture.
| Anterior grades | |
| A0 | No high-intensity area |
| A1 | Linear high-intensity area |
| A2 | Fusiform high-intensity area |
| Posterior grades | |
| P0 | No high-intensity area |
| P1 | High-intensity area not exceeding the nuchal ligament |
| P2 | High-intensity area exceeding the nuchal ligament |
Abbreviations: STIR, short T1 inversion recovery; MRI, magnetic resonance images; CSCI, cervical spinal cord injury.
The cervical spinal cord diameters at the center of the C3 vertebral body (A) and the injury intervertebral level (B) were measured using T2-weighted mid-sagittal MRI, as shown in Figure 3. 5 The narrowing rate of the spinal cord at the injury level for that at C3 was calculated as follows: (A-B) /A × 100. The narrowing rate was defined as the compression rate.
Figure 3.
Measurement of the compression rate using the T2-weighted mid-sagittal MRI. The spinal cord diameter at the center of the C3 vertebral body (A). The spinal cord diameter at the injury level (B).
Neurological Evaluations
Neurological evaluations were performed using the American Spinal Injury Association (ASIA) impairment scale (AIS) and the Japan Orthopedic Association (JOA) score at both the injury and the final follow-up. The AIS is a clinician-administered scale used to classify the severity (completeness) of injury in individuals with spinal cord injury as shown in Table 2. The JOA score is a scoring system that consists of seven items: motor functions of the upper and lower extremities, muscle weakness of the deltoid and/or the biceps brachii, sensory functions of the upper and lower extremities and trunk, and bladder function. Relationships between the STIR-MRI Grade and the neurological outcomes of the AIS and the JOA score were investigated.
Table 2.
ASIA Impairment Scale.
| A | Complete | No motor, sensory, sacral sparing |
| B | Incomplete | No motor, sensory only |
| C | Incomplete | 50% of muscles less than grade 3 (cannot raise arms or legs off bed) |
| D | Incomplete | 50% of muscles more than grade 3 (can raise arms or legs off bed) |
| E | Normal | Motor and sensory function are normal |
Abbreviation: ASIA, American Spinal Injury Association.
Statistical Analysis
Wilcoxon signed-rank tests were used to compare the JOA score at the injury and at the final follow up; differences with a P-value < 0.05 were considered statistically significant. The Kruskal-Wallis test was performed to assess the difference between the three groups (A0, A1, and A2 or P0, P1, and P2) in terms of the AIS, JOA score, and compression rate. If statistical significance (P < 0.05) was confirmed, a Mann-Whitney test was performed between pairs of groups. Using Bonferroni’s adjustment, a P-value < 0.0166 was considered the cut-off for statistical significance. All tests were conducted using SPSS Statistic Version 22 (IBM, Armonk, New York).
Ethical Approval
This study was approved by the institutional ethics committee of Odate Municipal General Hospital (approval number 30-09), and informed consent was obtained from all participants.
Results
Clinical and Demographic Characteristics
Overall, eight patients had spinous process fractures. The mean age of patients at the time of injury was 68 years (range, 31–91). Eleven patients had ossification of the posterior longitudinal ligament. Overall causes of CSCI were falling from a height (including stairs), falls from standing or seated heights, and traffic accidents in 16 (47%), 15 (44%), and three (9%) patients, respectively. The average follow-up period was 20 months (range, 12-84).
Distribution of the Patients According to the STIR-MRI Grade and Minor Fractures
All patients who were classified with A0 had P0 (Table 3). Six patients with P1 and two patients with P2 had spinous process fractures (Table 3). In term of the anterior grades, distributions of the patients as per A0 and A1 were similar (35% and 41%, respectively). However, distributions of the patients differed in the posterior grades (P0 50%, P1 35%, and P2 15%, Table 3).
Table 3.
Distribution of the Patients Based on the STIR-MRI Grade.a
| Posterior grades | |||||
|---|---|---|---|---|---|
| P0 | P1 | P2 | Total | ||
| Anterior grades | A0 | 12 | 0 | 0 | 12 (35%) |
| A1 | 3 | 7 (3) | 4 (1) | 14 (41%) | |
| A2 | 2 | 5 (3) | 1 (1) | 8 (24%) | |
| Total | 17 (50%) | 12 (35%) | 5 (15%) | 34 (100%) | |
Abbreviation: n, number of patients.
aValues in italic in parentheses are number of patients with spinous process fractures.
The Relationship between the Results of the STIR-MRI Grade and the Neurological Outcomes
Although one or more scale improvements in the AIS results were observed in 27 patients, no improvement was seen in seven patients (Table 4). In particular, all nine patients with scale C at the injury improved by one or more scale by the final follow-up (Table 4). Of 21 patients with scale D at the injury, 15 (71%) patients improved to scale E by the final follow-up (Table 4). Anterior grades did not relate to the AIS results at the injury and the final follow-up (Figure. 4). Among posterior grades at the injury, the AIS in P2 patients was significantly more severe (P = 0.007 and P = 0.015, respectively) than that in P0 patients at both the injury and the final follow-up (Figure 4). The AIS in P2 patients was significantly more severe (P = 0.008) than that in P1 patients at the injury (Figure 4). The AIS in P2 patients trended to be more severe (P = 0.030) than that in P1 patients at the final follow-up.
Table 4.
Distribution of Patients According to the ASIA Impairment Scale at the Injury and the Final follow-Up.
| Final follow-up | ||||||
|---|---|---|---|---|---|---|
| A | B | C | D | E | ||
| At the injury | A | 1 | − | 1 | − | − |
| B | − | − | 1 | 1 | − | |
| C | − | − | − | 5 | 4 | |
| D | − | − | − | 6 | 15 | |
Abbreviations: n, number of patients; ASIA, American Spine Injury Association.
aValues in bold are number of patients who had one or more grades improvement. Values in gray are the number of patients who had unchanged grades
Figure 4.
The relationships between the STIR-MRI Grade and the AIS. Upper: Relationships between the anterior grades and the AIS at the injury (a) and the final follow-up (b). Lower: Relationships between the posterior grades and the AIS at the injury (c) and the final follow-up (d). Differences with a P-value < 0.0166 were considered statistically significant.
The mean JOA score of 7.3 points at the injury significantly improved (P < 0.001) to 12.1 points at the final follow-up (Figure 5). Anterior grades were not related to the mean JOA score at either the injury or the final follow-up (Figure 6). In posterior grades at the final follow-up, however, the mean JOA score in P2 patients (3.9 points) was significantly lower (P = 0.016) than in P0 patients (13.6 points) (Figure 6). At the injury, the mean JOA score in P2 patients (1.4 points) was lower (P = 0.045) than in P0 patients (7.6 points) (Figure 6). At the final follow-up, the mean JOA score in P2 patients (3.9 points) was lower (P = 0.05) than in P1 patients (13.3 points) (Figure 6).
Figure 5.
The JOA score at the injury and the final follow-up. The mean JOA score of 7.3 ± 5.2 points at the injury significantly improved to 12.1 ± 5.7 points at the final follow-up (P < 0.001). Bold lines indicate the patients classified as P2 based on the STIR-MRI Grade. Differences with a P-value < 0.05 were considered statistically significant.
Figure 6.
Relationships between the STIR-MRI Grade and the JOA score at the injury and the final follow-up. Upper: Relationships between the anterior grades and the JOA score. Lower: Relationships between the posterior grades and the JOA score. Differences with a P-value < 0.0166 were considered statistically significant.
For all anterior grades of A0, A1, and A2, the mean JOA scores of 8.3, 6.0, and 8.0 points, respectively at the initial injury, significantly improved to 13.8, 10.6, and 12.1 points, respectively at the final follow-up (P = 0.003, P = 0.001, and P = 0.018, respectively, Table 5). Although the mean JOA scores in P0 and P1 of 7.6 and 9.3 points at the initial injury significantly improved to 13.6 and 13.3 points, respectively at the final follow-up (P < 0.001 and P = 0.003, respectively), the mean JOA score in P2 (1.4 points) at the injury did not significantly improve by the final follow-up (3.9 points) (Table 5).
Table 5.
The JOA Score Based on the STIR-MRI Grade.
| At the injury (points) | Final follow-up (points) | P -value | |
|---|---|---|---|
| Anterior grades | |||
| A0 (n = 12) | 8.3 ± 2.8 | 13.8 ± 2.9 | 0.003 |
| A1 (n = 14) | 6.0 ± 5.7 | 10.6 ± 6.3 | 0.001 |
| A2 (n = 8) | 8.0 ± 6.0 | 12.1 ± 6.9 | 0.018 |
| Posterior grades | |||
| P0 (n = 17) | 7.6 ± 3.4 | 13.6 ± 3.5 | < 0.001 |
| P1 (n = 12) | 9.3 ± 5.3 | 13.3 ± 5.0 | 0.003 |
| P2 (n = 5) | 1.4 ± 5.9 | 3.9 ± 6.7 | 0.068 |
Abbreviation: JOA, Japanese Orthopedic Association.
aThe values are shown as means ± standard deviation. Bold indicates a significant P-value.
The Relationship between the Finding of the STIR-MRI Grade and Compression Rate
For anterior grades, although the mean compression rate in A2 patients (19.1) was smaller than that in A0 and A1 patients (28.4 and 29.9, respectively), the difference was not significant. Likewise, in posterior grades, although the mean compression rate in P1 patients (22.0) was smaller than that in P0 and P2 patients (30.5 and 22.0, respectively), the difference was not significant. (Table 6 and Figure 7).
Table 6.
The Results of the Compression Rate Based on the STIR-MRI Grade.a
| STIR-MRI grade | Compression rate |
|---|---|
| Anterior grades | |
| A0 | 28.4 ± 11.9 |
| A1 | 29.9 ± 10.9 |
| A2 | 19.1 ± 8.7 |
| Posterior grades | |
| P0 | 30.5 ± 11.7 |
| P1 | 22.0 ± 11.2 |
| P2 | 26.1 ± 7.1 |
aThe values are shown as means ± standard deviation.
Figure 7.
Relationships between the STIR-MRI Grade and the compression rate. Relationships between the anterior (a) or the posterior (b) grades and the compression rate. Differences with a P-value < 0.0166 were considered statistically significant.
A Representative P2 Case for the STIR-MRI Grade
A 62-year-old man fell from the stairs, and he was brought to our hospital in an ambulance with neck pain and quadriplegia. We could detect HIA in the posterior paraspinal soft tissue on STIR mid-sagittal MRI in MRI evaluations, but not on the T2-weighted MRI, as shown in Figure 8. Based on the STIR-MRI Grade, he was graded as being A1 and P2 (Figure 8). At admission, his AIS was scale B. The JOA score was -2 points (upper-extremity motor: 0 points; muscle weakness of the deltoid and/or the biceps brachii: -2; lower-extremity motor: 0; upper-extremity sensory: 0; trunk sensory: 0; lower-extremity sensory: 0; and bladder function: 0). Since he had no major fractures and no dislocations, he was treated conservatively for more than 2 years after his injury. The AIS of scale B at the initial injury improved to scale D at the final follow-up. The JOA score of -0.2 points at the injury improved to 4.5 points at the final follow-up. However, numbness and severe motor deficit of both the upper extremities remained, and he required a walker to walk.
Figure 8.
A 62-year-old man after CSCI without major fracture. The T2-weighted mid-sagittal MRI did not show a high-intensity area in the posterior soft tissue (a). The STIR mid-sagittal MRI showed a high-intensity area which exceeded the nuchal ligament (arrows) (b).
Discussion
This study determined the relationship between the paraspinal soft tissue damage at the initial injury, which was evaluated using a new grading system based on the STIR mid-sagittal MRI, referred to as “STIR-MRI Grade”, and the neurological improvements after CSCI without major fracture. Although anterior grades based on the STIR-MRI Grade did not relate to neurological improvements, P2 based on the STIR-MRI Grade led to poor neurological improvements after CSCI without major fracture.
MRI is widely used to evaluate damage after CSCI.1-2,6-8 The high-signal change on MRI is useful for assessing the damage to the cervical spinal cord, the cervical spinal bone, and the paraspinal soft tissue and is used as a prognostic predictor of the neurological outcomes.1,2,9-13 The most common cause of CSCI without major fracture was reported to be a sudden neck hyperextension.14-16 The HIA of the anterior paraspinal soft tissue on MRI is also reported to reflect prevertebral hemorrhage caused by anterior longitudinal ligament and disc damage during sudden neck hyperextension. Kumagai et al. 2 and Machino et al. 3 measured the longitudinal length of prevertebral HIA on the T2-weighted mid-sagittal MRI in patients after CSCI and reported that there was no correlation between the results of longitudinal measurements of HIA and the JOA score at both the injury and the final follow-up. Conversely, Maeda et al. 1 measured the cross-sectional area of the prevertebral HIA on the T2-weighted mid-sagittal MRI in patients after CSCI and reported that a larger cross-sectional area of HIA led to severe paralysis in the ASIA motor score. Therefore, the evaluation methods of prevertebral bleeding using the T2-weighted MRI after CSCI varied, and it is still controversial whether prevertebral bleeding on T2-weighted MRI is significantly related to the neurological outcomes. In this study, STIR mid-sagittal MRI was used to evaluate the paraspinal soft tissue damage after CSCI without major fracture because fat tissue may also appear with a high-signal like oedema caused by soft tissue damage on the T2-weighted mid-sagittal MRI. Furthermore, the authors developed the STIR-MRI Grade, which qualitatively evaluates the paraspinal soft tissue damage. The STIR-MRI Grade has the following advantages: it is a prognostic indicator of the neurological improvements after CSCI without major fracture; it is easy to recognize the degree of the paraspinal soft tissue damage for qualitative evaluation; it is relatively easy to implement; and MRI is less invasive. In this study, although anterior grades in the STIR-MRI Grade were not related to the AIS and the JOA score, P2 in the posterior grades in the STIR-MRI Grade led to poor neurological outcomes based on the AIS and the JOA score.
STIR MRI was reported to be sensitive for detecting oedema and effective for diagnosing damage to the soft tissue and the interspinous or supraspinous ligaments. 4 Oichi et al. investigated the paraspinal soft tissue damage in 122 patients after CSCI using T2-weighted MRI and reported that the frequencies of anterior and posterior damage were 66% and 22%, respectively. 17 In this study using the STIR-MRI Grade, the frequencies of anterior (i.e., A1 or A2) and posterior damages (i.e., P1 or P2) damage to the soft tissue were 65% and 50%, respectively. Therefore, the STIR-MRI Grade can evaluate paraspinal soft tissue damage more clearly than the T2-weighted MRI, especially in posterior soft tissue. We speculate that an HIA exceeding the nuchal ligament in P2 may be due to hemorrhage caused by the disruption of the nuchal ligament or the fascia of posterior muscles connecting to the nuchal ligaments or the spinous process fracture.
The AOSpine subaxial cervical spine injury classification system (AOSpine SCICS) described injuries based on four criteria: (1) morphology of the injury (A: compression injuries, B: tension band injuries, C: translation injuries), (2) facet injury, (3) neurologic status, and (4) any case-specific modifiers (Table 7). 18 This system demonstrates substantial interobserver and intraobserver reliability in the initial assessment and is considered a valuable tool for communication, patient care, and research purposes.18,19 MRI is a useful tool in diagnosing posterior ligamentous complex (PLC) injury when CT does not reveal the destruction of bone structure.18,19 The PLC injury revealed by MRI would be classified as a modifier (M1) using the AOSpine SCICS and corresponds to P1 or P2 in the STIR-MRI Grade in this study. In particular, the presence of M1 in compression injury (Type A) has been reported to suggest the possibility of mechanical instability and to be useful in determining treatment strategies.20,21 However, the morphology of the injury is also different from the previous reports because this study targeted CSCI without major fracture. In addition, there was no mention of the range of high-signal changes on MRI in M1, the significance of M1 in tension band injury (Type B), or the relationship between M1 and neurological outcomes in the previous reports. All P1 or P2 (i.e., M1 of AOSpine SCICS) in this study were also associated with anterior paraspinal soft tissue damage that may reflect anterior longitudinal ligament and disc damage (Table 3). Specifically, it is presumed that the severe hyperextension injury caused the tensile failure of the anterior column and compressive failure of the posterior column. Furthermore, the presence of HIA exceeds the nuchal ligament in P2 in the STIR-MRI Grade significantly related to poor neurological outcomes. Therefore, the STIR-MRI Grade was considered a useful system because it may be possible to infer not only the morphology of the injury, but also the energy of the injury and neurological outcomes.
Table 7.
AOSpine Subaxial Cervical Spine Injury Classification System.
| Morphology of the injury | |
|---|---|
| Compression injuries | |
| A0 | Minor, nonstructural fractures |
| A1 | Wedge-compression |
| A2 | Split |
| A3 | Incomplete burst |
| A4 | Complete burst |
| Tension band injuries | |
| B1 | Posterior tension band injury (bony) |
| B2 | Posterior tension band injury (bony capsuloligamentous, ligamentous) |
| B3 | Anterior tension band injury |
| Translation injuries | |
| C | Translational injury in any axis-displacement or translation of one vertebral body relative to another in any direction |
| Facet injury | |
| F1 | Nondisplaced facet fracture |
| F2 | Facet fracture with potential for instability |
| F3 | Floating lateral mass |
| F4 | Pathologic subluxation or perched/ dislocated facet |
| BL | Bilateral injury |
| Neurological status | |
| N0 | Neurology intact |
| N1 | Transient neurologic deficit |
| N2 | Radicular symptoms |
| N3 | Incomplete spinal cord injury or any degree of cauda equina injury |
| N4 | Complete spinal cord injury |
| NX | Cannot be examined |
| Case-specific modifiers | |
| M1 | Posterior Capsuloligamentous Complex injury without complete disruption |
| M2 | Critical disc herniation |
| M3 | Stiffening/metabolic bone disease |
| M4 | Vertebral artery abnormality |
Several studies have reported that cervical spinal cord compression before injury is a risk factor for severe paralysis in patients after CSCI without bone fracture.1,3,5,17,22 Oichi et al. reported that a significant risk factor for severe paralysis was a spinal cord compression rate over 40% at the injury level. 17 Nakajima et al. reported that the ability to work was improved in the surgery group compared with the conservative group when the spinal cord compression rate was over 33.2%. 22 Conversely, several studies have reported no associations between cervical canal stenosis and neurological outcomes.1,5 In this study, there were no significant relationships between the compression rate and the AIS and the JOA score (data not shown). Although the differences were not significant, the compression rates in A2 and P1 were smaller than those in patients with other grades. Therefore, the patients classified as A2 or P1 may be injured due to high-energy exertion, even though they had lower cervical spinal cord compression rates before the injury.
The present study had several limitations. First, a small number of patients were enrolled. Second, the minimum follow-up period was only 1-year. Therefore, studies with a larger number of patients who are followed for a longer duration are necessary. Finally, there was no interobserver reliability. Since the STIR-MRI Grade is a prognostic indicator for neurological outcomes and injury energy, it is necessary to examine its precision in a larger group of patients.
Conclusions
Posterior grades using the STIR-MRI Grade were significantly related to neurological improvements using the AIS and the JOA score after CSCI without major fracture. The P2 STIR-MRI Grade was associated with poor neurological improvement using the AIS and the JOA score after CSCI. The STIR-MRI Grade can be used as a prognostic indicator for neurological improvements after CSCI without major fracture.
Footnotes
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.
ORCID iD: Kotaro Aburakawa, MD 
https://orcid.org/0000-0001-8236-9335
Kazunari Takeuchi, MD, PhD https://orcid.org/0000-0002-5480-3744
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