Predictors of intramedullary lesion expansion rate on MR images of patients with subaxial spinal cord injury

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OBJECT

Studies of preclinical spinal cord injury (SCI) in rodents indicate that expansion of intramedullary lesions (IMLs) seen on MR images may be amenable to neuroprotection. In patients with subaxial SCI and motor-complete American Spinal Injury Association (ASIA) Impairment Scale (AIS) Grade A or B, IML expansion has been shown to be approximately 900 μm/hour. In this study, the authors investigated IML expansion in a cohort of patients with subaxial SCI and AIS Grade A, B, C, or D.

METHODS

Seventy-eight patients who had at least 2 MRI scans within 6 days of SCI were enrolled. Data were analyzed by regression analysis.

RESULTS

In this cohort, the mean age was 45.3 years (SD 18.3 years), 73 patients were injured in a motor vehicle crash, from a fall, or in sport activities, and 77% of them were men. The mean Injury Severity Score (ISS) was 26.7 (SD 16.7), and the AIS grade was A in 23 patients, B in 7, C in 7, and D in 41. The mechanism of injury was distraction in 26 patients, compression in 22, disc/osteophyte complex in 29, and Chance fracture in 1. The mean time between injury onset and the first MRI scan (Interval 1) was 10 hours (SD 8.7 hours), and the mean time to the second MRI scan (Interval 2) was 60 hours (SD 29.6 hours). The mean IML lengths of the first and second MR images were 38.8 mm (SD 20.4 mm) and 51 mm (SD 36.5 mm), respectively. The mean time from the first to the second MRI scan (Interval 3) was 49.9 hours (SD 28.4 hours), and the difference in IML lengths was 12.6 mm (SD 20.7 mm), reflecting an expansion rate of 366 μm/ hour (SD 710 μm/hour). IML expansion in patients with AIS Grades A and B was 918 μm/hour (SD 828 μm/hour), and for those with AIS Grades C and D, it was 21 μm/hour (SD 304 μm/hour). Univariate analysis indicated that AIS Grade A or B versus Grades C or D (p < 0.0001), traction (p= 0.0005), injury morphology (p < 0.005), the surgical approach (p= 0.009), vertebral artery injury (p= 0.02), age (p < 0.05), ISS (p < 0.05), ASIA motor score (p < 0.05), and time to decompression (p < 0.05) were all predictors of lesion expansion. In multiple regression analysis, however, the sole determinant of IML expansion was AIS grade (p < 0.005).

CONCLUSIONS

After traumatic subaxial cervical spine or spinal cord injury, patients with motor-complete injury (AIS Grade A or B) had a significantly higher rate of IML expansion than those with motor-incomplete injury (AIS Grade C or D).

ABBREVIATIONSAIS= American Spinal Injury Association (ASIA) Impairment Scale; AMS= ASIA motor score; IML= intramedullary lesion; ISS= Injury Severity Score; MABP= mean arterial blood pressure; MCC= maximum canal compromise; MSCC= maximum spinal cord compression; SCI= spinal cord injury.

OBJECT

Studies of preclinical spinal cord injury (SCI) in rodents indicate that expansion of intramedullary lesions (IMLs) seen on MR images may be amenable to neuroprotection. In patients with subaxial SCI and motor-complete American Spinal Injury Association (ASIA) Impairment Scale (AIS) Grade A or B, IML expansion has been shown to be approximately 900 μm/hour. In this study, the authors investigated IML expansion in a cohort of patients with subaxial SCI and AIS Grade A, B, C, or D.

METHODS

Seventy-eight patients who had at least 2 MRI scans within 6 days of SCI were enrolled. Data were analyzed by regression analysis.

RESULTS

In this cohort, the mean age was 45.3 years (SD 18.3 years), 73 patients were injured in a motor vehicle crash, from a fall, or in sport activities, and 77% of them were men. The mean Injury Severity Score (ISS) was 26.7 (SD 16.7), and the AIS grade was A in 23 patients, B in 7, C in 7, and D in 41. The mechanism of injury was distraction in 26 patients, compression in 22, disc/osteophyte complex in 29, and Chance fracture in 1. The mean time between injury onset and the first MRI scan (Interval 1) was 10 hours (SD 8.7 hours), and the mean time to the second MRI scan (Interval 2) was 60 hours (SD 29.6 hours). The mean IML lengths of the first and second MR images were 38.8 mm (SD 20.4 mm) and 51 mm (SD 36.5 mm), respectively. The mean time from the first to the second MRI scan (Interval 3) was 49.9 hours (SD 28.4 hours), and the difference in IML lengths was 12.6 mm (SD 20.7 mm), reflecting an expansion rate of 366 μm/ hour (SD 710 μm/hour). IML expansion in patients with AIS Grades A and B was 918 μm/hour (SD 828 μm/hour), and for those with AIS Grades C and D, it was 21 μm/hour (SD 304 μm/hour). Univariate analysis indicated that AIS Grade A or B versus Grades C or D (p < 0.0001), traction (p= 0.0005), injury morphology (p < 0.005), the surgical approach (p= 0.009), vertebral artery injury (p= 0.02), age (p < 0.05), ISS (p < 0.05), ASIA motor score (p < 0.05), and time to decompression (p < 0.05) were all predictors of lesion expansion. In multiple regression analysis, however, the sole determinant of IML expansion was AIS grade (p < 0.005).

CONCLUSIONS

After traumatic subaxial cervical spine or spinal cord injury, patients with motor-complete injury (AIS Grade A or B) had a significantly higher rate of IML expansion than those with motor-incomplete injury (AIS Grade C or D).

ABBREVIATIONSAIS= American Spinal Injury Association (ASIA) Impairment Scale; AMS= ASIA motor score; IML= intramedullary lesion; ISS= Injury Severity Score; MABP= mean arterial blood pressure; MCC= maximum canal compromise; MSCC= maximum spinal cord compression; SCI= spinal cord injury.

Despite significant advances in methods of improving quality of life for people with spinal cord injury (SCI), full characterization of SCI and therapies to alter its course remain elusive. The importance of this condition is evidenced by the fact that every year, 12,000 people in the United States suffer an SCI, with an incidence of 40 per million. The worldwide population of people living with SCI is 2.5 million, resulting in immense personal burdens and societal costs.3,16,22,33,55,82 Although the means to reverse the initial damage to spinal cord tissues has yet to be discovered, halting the progression of the secondary injury at the molecular level seems promising.21,31,64,66,78,81

The results of preclinical studies in animal models indicate that SCI is not the result of a single static insult. Rather, it is a dynamic process defined by a distinctive cascade of molecular events after the initial trauma that creates a graded yet expansive intramedullary lesion (IML) that destroys spinal cord tissues, including endothelial cells, axons, myelin, and cell bodies.8,10,13,17,27,30,31,35,40,49,51,65,68 Unlike with motor-complete SCI, hematomyelia is absent in those with motor-incomplete SCI. These patients have axonal swelling and disruption in conjunction with minimal coagulative necrosis of the spinal cord parenchyma.1,2,24,26,46,53,59,75

As evident in experimental models of SCI,20,57,64 IML expansion in humans has yet to be fully validated.2 At the microscopic level, histopathological studies have shown that IML expansion occurs primarily within the first 24 hours after trauma.42,45,48 At the clinical level, analyses of MR images acquired during the first 6 days of injury have shown that patients with motor-complete SCI have significantly longer IMLs than patients with motor-incomplete injury.1,2,34,54,61 An attempt to characterize the temporal evolution of these IMLs in motor-complete (American Spinal Injury Association [ASIA] impairment scale [AIS] Grades A and B) subaxial cervical SCI through examination of serial MR images revealed that the rate of rostrocaudal expansion of IML occurred at approximately 900 μm/hour.2 Because of the differing clinical courses and outcomes in motor-incomplete SCI (AIS Grades C and D), we sought to verify the rate of IML expansion in this patient population and compare it to the rate found in patients with motor-complete SCI. To our knowledge, no study has examined serial MR images of humans with motor-incomplete SCI.

Because the final IML size seems to correlate with motor function, the ability to halt IML expansion and ultimately reduce the extent of injury can potentially lead to decreased morbidity from SCI. In vivo rodent models of SCI indicate that IML expansion can be mitigated by chemotherapeutic agents.50,56,57,64 T hus, f ull c haracterization of IML expansion and identification of factors influencing its progression may help identify medical and surgical interventions that could alter the course of SCI and result in improved clinical outcomes.2,64 Our hypothesis was that in patients with subaxial cervical spine trauma and SCI, IML expansion remains constant across all AIS grades.

Methods

Design

This was a retrospective analysis of prospectively collected data.

Primary Outcome

We studied the IML expansion rate on MR images of patients with subaxial cervical SCI.

Selection Criteria

Inclusion Criteria

To be included in the study, patients had to have had the following: 1) age older than 15 years, 2) a blunt trauma resulting in subaxial cervical spine fracture dislocations and SCI, 3) diagnosis of an AIS Grade A, B, C, or D injury, and 4) good-quality postresuscitation and postoperative (up to 6 days postinjury) CT and MRI scans (with distinct IML borders) of the cervical spine available.

Exclusion Criteria

Excluded were patients who had the following: 1) a penetrating cervical spine and spinal cord injury, 2) AIS Grade E, 3) traumatic brain injury, 4) only 1 MRI scan or only CT myelograms, 5) a nontraumatic central cord syndrome, and 6) neurological worsening during the study period.

Institutional Review Board Approval

This study was approved by the institutional review board of the University of Maryland School of Medicine.

Management Process

Emergency Medical, Prehospital, Trauma Center, and Critical Care Management

Emergency medical, transportation, trauma resuscitation unit, and inpatient critical care management of patients with SCI was performed according to the guidelines of the Maryland Institute for Emergency Medical Services System and the Congress of Neurological Surgeons/American Association of Neurological Surgeons–approved guidelines for the management of cervical spine and spinal cord injury.4,9,41

Clinical Evaluation and Imaging (CT and MRI) Studies

After patients were resuscitated by volume expansion and blood pressure augmentation73 and considered stable, primary and secondary surveys were performed by medical and surgical staff of the trauma center. Each patient was examined by the neurosurgical staff (attending physician, senior resident, or nurse practitioners) to determine the ASIA motor score (AMS) and AIS grade.76 Each patient was then transported to undergo CT scanning of the cervical spine and CT angiography.1,2 CT was used to assign a mechanistic phylogeny and stage for each patient according to Allen et al.7 After the CT scan, each patient underwent MRI studies of the cervical spine. Patients with electromagnetically activated implants or those with metallic foreign bodies near the spinal column incompatible with MRI underwent CT myelography to rule out the need for spinal cord decompression. Subjects with an intrinsic spinal cord lesion and no spinal cord compression underwent preoperative MRI only; however, those who underwent surgery for spinal cord decompression routinely had at least 1 postoperative MRI scan to verify spinal cord decompression.

Calculation of Maximum Canal Compromise, Maximum Spinal Cord Compression, and IML Expansion Rate

We used T2-weighted images or STIR sequences to determine maximum canal compromise (MCC) and maximum spinal cord compression (MSCC), as originally reported by Fehlings et al. and validated in several independent investigations.28,29,38,39,54 The mean interval from the injury to the time of acquisition of the first MRI scan was 10 hours (SD 8.7 hours; range 3–67.2 hours); this period was called Interval 1. The second MRI scan was performed a mean of 60 hours (SD 29.6 hours; range 15–134 hours) after trauma; this time period was called Interval 2. The mean time between the first and second MRI studies was 49.9 hours (SD 28.4 hours; range 9–124 hours) and was called Interval 3. MRI after trauma was used to determine the following parameters: 1) the IML length at the end of Interval 1 (IML1, in millimeters); 2) the sagittal diameter of the spinal canal at the site of skeletal injury (Di, in millimeters); 3) the MCC at the site of injury (in percent); and 4) the MSCC at the site of injury (in percent). The MCC and MSCC were calculated as follows using previously validated formulas:29,39

article image

where Di is the subaxial cervical spine sagittal diameter at the level of injury, Da is the midsagittal diameter of the spinal canal 1 or 2 motion segments above the level of injury, and Db is the midsagittal diameter of the spinal canal 1 or 2 motion segments below the level of spinal injury. The MSCC was calculated according to the following formula:

article image

where da is the diameter of the spinal cord at a normal segment above the level of SCI, db is the diameter of the spinal cord at a segment below the level of SCI, and di is the diameter of the spinal cord at the level of SCI (Fig. 1).

The second MRI scans were used to measure the rostrocaudal IML length at the end of Interval 2 (IML2, in millimeters). The rate of IML expansion was calculated according to the following formula:

article image
FIG. 1.
FIG. 1.

Midsagittal reformatted STIR image obtained 8.5 hours after trauma in a 27-year-old man who was involved in an automobile accident and sustained a C-6 teardrop fracture that resulted in quadriplegia. On admission, his AMS was 27 and his AIS grade was A. He underwent circumferential realignment, decompression, and internal fixation 20 hours after the trauma. The image indicates the Da, Di, Db, da, di, and db, parameters that were used to calculate the MCC and MSCC. The patient continued to have an AMS of 28 and AIS grade of A 11 months after the trauma. See Calculation of Maximum Canal Compromise, Maximum Spinal Cord Compression, and IML expansion Rate for the full explanation.

Medical Management

Each patient's postresuscitation mean arterial blood pressure (MABP) was kept at approximately 85 mm Hg for 7 days, as recommended, unless not medically advised because of comorbidities or age.14,52,73 Methylprednisolone for SCI was part of our medical management protocol from 2005 to 2010.44,63 Medical management was continued for each patient in the critical care or intermediate care facility until he or she was discharged to a rehabilitation center.

Closed Reduction

Patients with unilateral or bilateral facet dislocations (flexion distraction Stage 2 or 3) and those with significant compressive flexion injuries (teardrop fractures) underwent attempted closed reduction as a preliminary step before definitive spinal cord decompression. Closed reduction was not attempted for facet subluxations, Chance fractures, or extension injuries. In the majority of patients, closed reduction was performed after the admission CT and MRI studies. It is our practice to apply 5–7 lbs of traction per motion segment (counting from C-1) to complete closed reduction within a maximum interval of 1–2 hours.

Surgery

The surgical procedure prescribed for each individual patient was determined by the injury severity, morphology according to Allen's classification, and the presence of spinal instability.7,72 Overall, each patient with a facet dislocation, a teardrop fracture, or a vertical distraction injury underwent surgery via a circumferential approach to ensure that the construct being placed did not fail over time. Any patient with an extension-distraction injury associated with disc/osteophyte complexes or spinal stenosis underwent decompression and fusion via either an anterior or posterior approach alone, because there were usually no associated facet subluxations or dislocations.25,30,50,79

Follow-Up

After acute care and discharge, each patient was followed up to record the full degree of his or her neurosurgical recovery. The majority of the patients were followed up at institutions affiliated with the University of Maryland School of Medicine.

Safeguard for Bias

Selection bias was prevented by controlling for the following variables: MRI and surgical intervention intervals, age, sex, mechanism of injury, Injury Severity Score (ISS), admission and follow-up AMS and AIS grade, Allen et al. morphology phylogenies, vertebral artery injury, MCC, MSCC, closed reduction, steroid protocol, and surgical technique.74

Statistical Analysis

We report descriptive statistics as the mean and SD for continuous variables and frequencies and proportions for categorical variables. First, a univariate analysis was conducted to assess the association between any independent variable and the IML expansion rate. Because of the small sample sizes and nonnormal distribution of the outcome variable, a Mann-Whitney U-test or Kruskal-Wallis test was used to examine the association between the IML expansion rate and the categorical independent variables. In addition, a Spearman correlation was used to assess the correlation between the IML expansion rate and the other continuous variables. Finally, we performed a multiple regression analysis to assess the relationships between the IML expansion rate and the independent variables that were significant in the univariate analysis. We used the statistical program Stata SE/12.1 (release 12; Stata Corp LP) for analysis.

Results

From January 2005 to December 2012, 984 patients were admitted to the University of Maryland R Adams Cowley Shock Trauma Center with traumatic subaxial cervical SCI, of whom 78 consecutive subjects were eligible for our study. Table 1 lists the baseline characteristics of these patients along with the injury classifications and management variables. Under the mechanisms of injury in Table 1, the “other” category includes assault and battery in 3 patients and fall of heavy object on the head in 2 patients. On the basis of their AIS grade, we categorized the patients as having motor-complete SCI or motor-incomplete SCI.

TABLE 1

Characteristics of 78 patients with motor-complete and motor-incomplete subaxial SCIs

VariableAll PatientsPatients w/ Motor-Complete SCIPatients w/ Motor-Incomplete SCI
No. of patients783048
Male sex (no. [%])60 (77)26 (86.7)34 (71)
Age (mean [SD]) (yrs)45.3 (18.3)33.1 (12.8)52.8 (17.1)
Mechanism (no. [%])
 Motor vehicle crash30 (38.5)17 (56.7)13 (27)
 Fall26 (33.3)5 (16.7)21 (43.8)
 Sport17 (21.8)6 (20)11 (23)
 Other5 (6.4)2 (6.7)3 (6.3)
Admitting ASIA motor score (mean [SD])53.6 (35.2)14.4 (11.5)78.1 (18.8)
AIS grade (no. [%])
 A23 (29.5)23 (76.7)0 (0.0)
 B7 (9)7 (23.3)0 (0.0)
 C7 (9)0 (0.0)7 (14.6)
 D41 (52.6)0 (0.0)41 (85.4)
Injury severity
 ISS (mean [SD])26.7 (16.7)41.5 (17.7)17.3 (5.4)
 Morphology of injury (no. [%])
  Distraction26 (33.3)16 (53.3)10 (20.8)
  Compression22 (28.2)12 (40.0)10 (20.8)
  Disc/osteophyte complex29 (37.2)2 (6.7)27 (56.3)
  Other1 (1.3)0 (0)1 (2.1)
 Subaxial sagittal diameter (mean [SD]) (mm3)6.8 (2)7.1 (2.4)6.7 (1.7)
 MCC (mean [SD]) (%)42.2 (14)45.9 (16.4)39.9 (12.3)
 MSCC (mean [SD]) (%)7.5 (22)5.7 (30.6)8.6 (15.1)
IML length (mean [SD]) (mm)
 During Interval 138.8 (20.4)59.0 (15.3)26.3 (10.8)
 During Interval 251 (36.5)87.4 (33.5)28.2 (11.3)
IML expansion rate (mean [SD]) (mm/hr)366 (712)920 (820)20 (340)
Management (no. [%])
 Surgical approach
  Anterior24 (30.7)4 (13.3)20 (41.7)
  Posterior10 (12.8)1 (3.3)9 (18.8)
  Circumferential44 (56.5)25 (83.3)19 (39.6)
 Steroids47 (60)25 (83.3)22 (45.8)
Outcome
 AMS at follow-up (mean [SD])69.1 (37)22 (17.5)94.6 (8.5)
 AIS grade at follow-up* (no. [%])
  A22 (28.2)22 (81.5)0 (0)
  B5 (6.5)5 (18.5)0 (0.0)
  C2 (2.5)0 (0.0)2 (3.9)
  D40 (51.3)0 (0)40 (78.4)
  E9 (11.5)0 (0)9 (17.7)
Mean follow-up (mos)21.41531

Because of their improved conditions, some patients' grades were different at follow-up (motor-complete SCI, n= 27; motor-incomplete SCI, n= 51).

Volume Expansion and Blood Pressure Augmentation

Of our 78 patients, 73 had detailed vital signs recorded for the entirety of the period between arrival and the second MRI scan. Of these 73 patients, 22 (30%) had at least 1 episode of an MABP of < 60 mm Hg for at least 15 minutes. Fifty-one patients (70%) had a stable MABP (≥ 60 mm Hg) for the time interval of interest. The average IML expansion was 340 μm/hour (SD 710 μm/hour) in patients with evidence of assumed ischemic episodes and 410 μm/ hour (SD 737 μm/hour) in patients without evidence of ischemic episodes. This difference was not statistically significant (p= 0.41).

CT Scanning and CT Angiography

Fourteen (18%) of 78 patients did not undergo vascular studies. Of the remaining 64 patients, 19 (30%) showed evidence of vertebral artery injury. Vertebral artery injury was on the left side in 7, on the right side in 6, and bilateral in 6 patients. Injury was Grade IV in 14, Grade III in 1, Grade II in 2, and Grade I in 2 patients. The average IML expansion rate was 560 μm/hour (SD 802 μm/hour) in patients with vertebral artery injury and 390 μm/hour (SD 743 μm/hour) in patients without vertebral artery injury. Univariate statistical analysis indicated that this difference was significant (p= 0.02); however, this difference lost its statistical value in multivariate regression analysis.

MRI Studies

In this investigation, 2 patients underwent CT myelography and 49 patients had an intrinsic spinal cord lesion without spinal cord compression. These patients did not undergo postoperative MRI studies and were excluded from the study. When the IML expansion rate was plotted against the timing of the first MRI acquisition, it was evident that the rate of expansion was faster closer to the time of trauma. The exact time of onset of IML expansion could not be determined from our retrospective data (Fig. 2).

FIG. 2.
FIG. 2.

Scatter plot demonstrating the relationship between the IML expansion rate and the time past injury to the first MRI scan (Interval 1). The expansion rate increases as the MR image acquisition approaches the time of trauma.

Steroid Protocol

Of the 78 patients in our study, 31 did not receive the steroid protocol, whereas 47 did (30 mg/kg/hour for 15 minutes and 5.4 mg/kg/hour for 24 hours).15 The average rate of IML expansion was 300 μm/hour in patients treated with steroids and 409 μm/hour in patients not treated with steroids. This difference did not achieve statistical significance (p= 0.198).

Closed Reduction

Of our 78 patients, traction was not applicable in the 29 patients with SCI because of extension injuries with disc/ osteophyte complexes or in the 1 patient with a Chance fracture. Of the 26 patients with distraction injuries, 14 underwent closed reduction, which was successful in 8 patients. Of the 22 patients with compression fractures, 3 underwent closed reduction, all of which were successful. The average IML expansion rate was 880 μm/hour (SD 900 μm/hour) in patients who had traction and 220 μm/hour (SD 580 μm/hour) in patients who did not have traction. Univariate statistical analysis indicated that this difference was significant (p= 0.0005). The significance, however, was lost in multivariate regression analysis.

Surgical Decompression

Of our 78 patients, the exact time interval between the injury and surgery was unknown for 6 patients. In the remaining 72 patients, 45 (62.5%) underwent surgical intervention less than 24 hours after the trauma, and 27 (37.5%) underwent surgical intervention 24 hours or more after injury. The mean IML rates of expansion in the first and second groups were 500 μm/hour and 190 μm/hour, respectively. Although this difference seems considerable (p < 0.05, univariate analysis), in the multivariate regression analysis, the interval between injury and surgery did not have a statistically significant effect on the rate of lesion expansion.

In this study, anterior, posterior, and circumferential surgical approaches were used in 24, 10, and 44 patients, respectively. The mean IML expansion rates were 152 μm/hour (SD 345 μm/hour) in patients who underwent either the anterior or posterior surgical approach and 532 μm/hour (SD 867 μm/hour) in those who underwent the circumferential surgical approach. Univariate statistical analysis indicated that this difference was significant (p= 0.009); however, the significance was lost in the multivariate regression statistical analysis.

AIS Grade

The mean rostrocaudal IML lengths seen on the first and second MRI scans were 38.8 mm (SD 20.4 mm) and 51 mm (SD 36.5 mm), resulting in a difference in lesion length of 12.6 mm (SD 20.7 mm) between the 2 scans. As a result, the mean IML expansion rate was found to be 366 μm/hour (SD 710 μm/hour) for the entire cohort. When lesion expansion was analyzed separately for patients with motor-complete (AIS Grade A or B) and motor-incomplete (AIS Grade C or D) SCI, the rate was significantly different. The mean rate of lesion expansion in patients with AIS Grade A or B was found to be 918 μm/hour (SD 828 μm/hour), whereas that in those with AIS Grade C or D was much lower (21 μm/hour [SD 304 μm/hour]). In comparison with the rapid rate of expansion seen in patients with motor-complete SCI, the rate in patients with motorincomplete SCI was nearly static and even showed regression in some patients.

Case 1

A 20-year-old woman sustained injury in a motor vehicle crash and was admitted to our center with an AMS of 89 and AIS grade of D. CT scanning revealed a C-6 compressive flexion Stage 3 injury. The IML length on the admission MR images, acquired 14.4 hours after the accident, was 32.0 mm, and the IML length in the second MR images, acquired 64.8 hours after injury, was 35.9 mm. The rate of IML expansion was 80 μm/hour. Forty-two months after the trauma, her AMS was 99 and AIS grade was D (Fig. 3).

FIG. 3.
FIG. 3.

Midsagittal reformatted CT and MR images of the cervical spine of a 20-year-old woman admitted to the trauma resuscitation unit after an automobile accident with an AMS of 89 (AIS Grade D). Forty-two months after decompression and circumferential internal fixation, her AMS was 99 and her AIS grade was D. A: Teardrop compression fracture of C-6 (white arrow). B: A lesion 32 mm long with high signal intensity 14.4 hours after the trauma (bracket 1). C: At 64.8 hours after the injury and after decompression, realignment, and internal fixation, her MR image showed a high-intensity signal that was 35.9 mm long (bracket 2). The IML expansion rate in this patient was 80 μm/hour.

Case 2

While trimming a tree branch, a 25-year-old man sustained a C-5 teardrop (compressive flexion Allen Stage 4)7 fracture and became quadriplegic. His admission AMS was 12 and AIS grade was A. The IML length on the admission MR images, acquired 4.5 hours after injury, was 76.2 mm, and the IML length on the postoperative MR images acquired 44 hours after admission was 205.9 mm. The rate of expansion was 3200 μm/hour (Fig. 4).

FIG. 4.
FIG. 4.

Midsagittal preoperative (A and B) and postoperative (C and D) CT and MR images of a 25-year-old man who sustained a traumatic C-5 compression fracture. At the time of admission, his AMS was 12 and his AIS grade was A. Ten months after injury, he remained quadriplegic. Shown are a C-5 teardrop fracture (A) (white arrow), a preoperative MR image 4.5 hours after injury with an intramedullary high-intensity signal measuring 76.2 mm in length (B) (bracket E), a postoperative CT image (C), and a postoperative MR image 44 hours after injury demonstrating an IML measuring 259 mm in length (D) (bracket F). The IML expansion rate was 3200 μm/hour.

Statistical Findings

Univariate analysis of 9 prognostic indicators revealed that age (p= 0.05; Fig. 5), ISS (p= 0.05), admission AMS (p= 0.05; Fig. 6), time between injury and surgery (p= 0.05; Fig. 7), injury morphology (p= 0.005; Fig. 8), and SCI severity (AIS Grade A or B vs AIS Grade C or D, p < 0.0001; Fig. 9) affected the IML expansion rate. When analyzed by regression analysis, however, only AIS grade significantly influenced the IML expansion rate (p= 0.005) (Table 2).

FIG. 5.
FIG. 5.

Scatter plot illustrating a progressive decline in IML expansion with increased patient age.

FIG. 6.
FIG. 6.

Scatter plot demonstrating the relationship between the IML expansion rate and AMS at admission. Lower AMSs tended to have faster IML expansion rates.

FIG. 7.
FIG. 7.

Scatter plot depicting the relationship between time to surgery and the IML expansion rate.

FIG. 8.
FIG. 8.

Histogram showing the relationship between injury morphology and the IML expansion rate. DISC/OST= disc/osteophyte complex.

FIG. 9.
FIG. 9.

Histogram illustrating the relationship between AIS grade and the IML expansion rate.

TABLE 2

Multiple regression model indicating significance of multiple independent variables as predictors of the IML rate of expansion

Independent VariableCoefficient (95% CI)p Value
Age0.0056 (−0.0065 to 0.0179)0.93
ISS−0.0022 (−0.0148 to 0.0102)0.718
AMS−0.0002 (−0.0095 to 0.0090)0.956
TPI to surgery0.0022 (−0.0051 to 0.0096)0.546
Accidental fall−0.1303 (−0.5231 to 0.2625)0.510
Sport injury0.0239 (−0.3471 to 0.3949)0.898
Compression injury0.631 (−0.3765 to 0.5029)0.775
Disc-osteophyte injury−0.0045 (−0.4252 to 0.4161)0.983
Traction0.1932 (−0.1572 to 0.5436)0.275
AIS Grades A & B vs Grades C & D1.0452 (0.3244 to 1.769)0.005*
Constant−0.2618 (1.2950 to 0.7714)0.614
CI= confidence interval; TPI= time past injury.

Statistically significant.

Discussion

Analyses of the data from this investigation indicate that AIS grade significantly influences the lesion expansion rate after traumatic SCI.

Light and electron microscopic studies in animal models of traumatic SCI by Dohrmann et al. and Wagner et al.23,24,75 indicated that within 5 minutes of a compressive and contusive SCI, congestion of venules in the capillaryrich central gray matter was followed by a break in endothelial integrity and extravasation of red blood cells, producing hematomyelia. Microangiographic studies by Fairholm and Turnbull26 r evealed a fl uffy e xtravasation of contrast material in the central part of the spinal cord within 10 minutes.5,6,23,24,26,69,70,75 From 4 to 7 days after SCI, capillary perfusion in the central gray matter was disrupted permanently and replaced by myelomalacia and coagulative necrosis.25 Numerous preclinical studies have indicated that immediately after SCI, the disruption of endothelial cells, axons, and the cytoskeleton, in association with molecular cascades and ionic imbalances, results in cytotoxic and vasogenic spinal cord edema, collectively labeled “secondary injury.”11–13,17–19,26,35,36,43,62,65,67,68

The results of combined MRI and necropsy investigations by Quencer et al.,59 Jimenez et al.,46 and Martin et al.53 of patients who d ied within a few d ays a fter a cute traumatic central cord syndrome indicated that axonal swelling and disruption in association with minimal coagulative necrosis of gray matter are visualized as a highintensity signal IML on T2-weighted MR images. These patients with partial SCI did not show hematomyelia in histological sections. Similarly, none of the patients with AIS Grade C or D in our investigation had hematomyelia on MRI. In contrast, studies of patients with complete subaxial SCI since the 1990s have clearly depicted associated intramedullary hematomyelia and swelling, as seen in our investigation in the patients with motor-complete SCI.1,2,34,54,60,61 Hematomyelia was often seen in complete SCI in association with an IML length that exceeded a single motion segment in the studies of Flanders et al.,34 Schaefer et al.,61 and Miyanji et al.,54 who demonstrated a relationship between injury severity and IML length.2 In 2007, Miyanji et al.54 reported on t he I ML length i n patients with complete versus those with incomplete SCI. In their study, IML length was approximately 20 mm in incomplete injuries and reached up to 40 mm in complete injuries. Further expansion of this concept was seen in 2012, when Aarabi et al.2 reported that IML length on MR images is a dynamic phenomenon with an expansion rate of 900 μm/hour. In the present investigation, applying a regression model to control for age, ISS, inpatient hypotensive episodes, injury morphology, vertebral artery injuries, performance of closed reduction, steroid protocol, operative technique, and the timing of decompression, the expansive character of the IML in patients with motor-complete SCI was validated to be close to 920 μm/hour. To our surprise, however, in patients with motor-incomplete SCI (AIS Grades C and D), the IML length-expansion rate was almost static (20 μm/hour; Fig. 9) without the aggressive expansive character observed in patients with motorcomplete SCI (AIS A and B).

In vivo preclinical MRI studies by Nout et al.,57 Chou et al.,20 and Simard et al.64 indicated that not only is an IML clearly demonstrated in experimental animals, but expansion of the lesion may also respond to neuroprotection.37 In those investigations, hypertonic saline, S-nitrosoglutathione, and glibenclamide slowed the progression of the molecular cascades seen in secondary injury, thereby shortening the final IML length. Our present investigation supports the notion that secondary injury may be much more intense in patients with motor-complete SCI than in those with incomplete SCI and may require the initiation of more aggressive neuroprotection at an earlier time to attenuate IML expansion.

Considering the nearly static nature of the IML in motorincomplete subaxial cervical SCI, one possible implication of this study is the potential difference between patients with motor-incomplete and those with motor-complete SCI in terms of level of urgency for neuroprotection and timing of decompression. Many of the exigencies considered vital for the management of motor-complete SCIs, such as early initiation of therapy for neuroprotection and the timing of decompression, may not apply to motor-incomplete SCI as well as to acute traumatic central cord syndrome.1,58,71,73 In addition, the seemingly significant effects manifested by traction, the timing of decompression, and surgical technique may simply reflect increased injury severity contributing to greater spinal cord swelling and a faster IML expansion rate.32,47,77,79,80

There are limitations to this study. Because the study was retrospective, the allocation of Intervals 1, 2, and 3 to patients was inherently heterogeneous. Also, considering the small number of patients and their uneven distribution in each category, statistical findings should be interpreted with caution. The findings of this investigation should be validated by a prospective multicenter study.

Conclusions

The results of previous MRI studies of patients with SCI suggest that those with incomplete SCI do not harbor hematomyelia; instead, the high-intensity signal seen on MR images is indicative of swollen and interrupted axons, primarily in the dorsolateral funiculi of the involved spinal cord segments. In addition, IML length has been reported to be longer in patients with motor-complete SCI. Further expanding on these previous findings, results of the present investigation indicate that the IML in motor-complete SCI expands aggressively in association with significant swelling, whereas the IML in patients with motor-incomplete SCI is almost static with little expansion, and in some cases regression, over time. One potential implication of these findings is that the pursuit of neuroprotection should be more aggressive and earlier to interrupt the expansion of the molecular cascades forming the foundation of secondary injury.

Author ContributionsConception and design: Aarabi. Acquisition of data: Aarabi, Le, Hersh, Shanmuganathan, Diaz, Massetti. Analysis and interpretation of data: Aarabi, Akhtar-Danesh. Drafting the article: Aarabi, Le. Critically revising the article: Aarabi, Le, Akhtar-Danesh. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Aarabi. Statistical analysis: Aarabi, Akhtar-Danesh. Administrative/technical/material support: Aarabi. Study supervision: Aarabi. Oversight for the scientific foundation and data safety and monitoring: Aarabi.

References

  • 1

    Aarabi BAlexander MMirvis SEShanmuganathan KChesler DMaulucci C: Predictors of outcome in acute traumatic central cord syndrome due to spinal stenosis. J Neurosurg Spine 14:1221302011

    • Search Google Scholar
    • Export Citation
  • 2

    Aarabi BSimard JMKufera JAAlexander MZacherl KMMirvis SE: Intramedullary lesion expansion on magnetic resonance imaging in patients with motor complete cervical spinal cord injury. J Neurosurg Spine 17:2432502012

    • Search Google Scholar
    • Export Citation
  • 3

    Ackery ATator CKrassioukov A: A global perspective on spinal cord injury epidemiology. J Neurotrauma 21:135513702004

  • 4

    Alexander RHProctor HJ: Advanced Trauma Life Support (ATLS) Program for Physicians ChicagoAmerican College of Surgeons1993

  • 5

    Allen AR: Remarks on the histopathological changes in the spinal cord due to impact. An experimental study. J Nerve Ment Dis 41:1411471914

    • Search Google Scholar
    • Export Citation
  • 6

    Allen AR: Surgery of experimental lesion of spinal cord equivalent to crush injury of fracture dislocation of spinal column: a preliminary report. JAMA 57:8788801911

    • Search Google Scholar
    • Export Citation
  • 7

    Allen BL JrFerguson RLLehmann TRO'Brien RP: A mechanistic classification of closed, indirect fractures and dislocations of the lower cervical spine. Spine (Phila Pa 1976) 7:1271982

    • Search Google Scholar
    • Export Citation
  • 8

    Amar APLevy ML: Pathogenesis and pharmacological strategies for mitigating secondary damage in acute spinal cord injury. Neurosurgery 44:102710401999

    • Search Google Scholar
    • Export Citation
  • 9

    American College of Surgeons: Advanced Trauma Life Support (ATLS) ed 7ChicagoAmerican College of Surgeons2004

  • 10

    Anderberg LAldskogius HHoltz A: Spinal cord injury—scientific challenges for the unknown future. Ups J Med Sci 112:2592882007

    • Search Google Scholar
    • Export Citation
  • 11

    Anderson DK: Chemical and cellular mediators in spinal cord injury. J Neurotrauma 9:1431461992

  • 12

    Anthes DLTheriault ETator CH: Ultrastructural evidence for arteriolar vasospasm after spinal cord trauma. Neurosurgery 39:8048141996

    • Search Google Scholar
    • Export Citation
  • 13

    Baptiste DCFehlings MG: Pharmacological approaches to repair the injured spinal cord. J Neurotrauma 23:3183342006

  • 14

    Blood pressure management after acute spinal cord injury. Neurosurgery 50:3 SupplS58S622002

  • 15

    Bracken MBShepard MJHolford TRLeo-Summers LAldrich EFFazl M: Administration of methylprednisolone for 24 or 48 hours or tirilazad mesylate for 48 hours in the treatment of acute spinal cord injury. Results of the Third National Acute Spinal Cord Injury Randomized Controlled Trial. JAMA 277:159716041997

    • Search Google Scholar
    • Export Citation
  • 16

    Buchanan LEDitunno JF JrOsterholm JLCotler JMStaas WE Jr: Spinal cord injury: a ten-year report. Pa Med 93:36391990

  • 17

    Cadotte DWFehlings MG: Spinal cord injury: a systematic review of current treatment options. Clin Orthop Relat Res 469:7327412011

    • Search Google Scholar
    • Export Citation
  • 18

    Carlson GDWarden KEBarbeau JMBahniuk EKutina-Nelson KLBiro CL: Viscoelastic relaxation and regional blood flow response to spinal cord compression and decompression. Spine (Phila Pa 1976) 22:128512911997

    • Search Google Scholar
    • Export Citation
  • 19

    Carlson SLParrish MESpringer JEDoty KDossett L: Acute inflammatory response in spinal cord following impact injury. Exp Neurol 151:77881998

    • Search Google Scholar
    • Export Citation
  • 20

    Chou PCShunmugavel AEl Sayed HDesouki MMNguyen SAKhan M: Preclinical use of longitudinal MRI for screening the efficacy of S-nitrosoglutathione in treating spinal cord injury. J Magn Reson Imaging 33:130113112011

    • Search Google Scholar
    • Export Citation
  • 21

    Chow DSTeng YToups EGAarabi BHarrop JSShaffrey CI: Pharmacology of riluzole in acute spinal cord injury. J Neurosurg Spine 17:1 Suppl1291402012

    • Search Google Scholar
    • Export Citation
  • 22

    Devivo MJ: Epidemiology of traumatic spinal cord injury: trends and future implications. Spinal Cord 50:3653722012

  • 23

    Dohrmann GJWagner FC JrBucy PC: The microvasculature in transitory traumatic paraplegia. An electron microscopic study in the monkey. J Neurosurg 35:2632711971

    • Search Google Scholar
    • Export Citation
  • 24

    Dohrmann GJWagner FC JrBucy PC: Transitory traumatic paraplegia: electron microscopy of early alterations in myelinated nerve fibers. J Neurosurg 36:4074151972

    • Search Google Scholar
    • Export Citation
  • 25

    Dvorak MFFisher CGFehlings MGRampersaud YROner FCAarabi B: The surgical approach to subaxial cervical spine injuries: an evidence-based algorithm based on the SLIC classification system. Spine (Phila Pa 1976) 32:262026292007

    • Search Google Scholar
    • Export Citation
  • 26

    Fairholm DJTurnbull IM: Microangiographic study of experimental spinal cord injuries. J Neurosurg 35:2772861971

  • 27

    Fehlings MGBaptiste DC: Current status of clinical trials for acute spinal cord injury. Injury 36:Suppl 2B113B1222005

  • 28

    Fehlings MGFurlan JCMassicotte EMArnold PAarabi BHarrop J: Interobserver and intraobserver reliability of maximum canal compromise and spinal cord compression for evaluation of acute traumatic cervical spinal cord injury. Spine (Phila Pa 1976) 31:171917252006

    • Search Google Scholar
    • Export Citation
  • 29

    Fehlings MGRao SCTator CHSkaf GArnold PBenzel E: The optimal radiologic method for assessing spinal canal compromise and cord compression in patients with cervical spinal cord injury. Part II: Results of a multicenter study. Spine (Phila Pa 1976) 24:6056131999

    • Search Google Scholar
    • Export Citation
  • 30

    Fehlings MGVaccaro AWilson JRSingh ACadotte WDHarrop JS: Early versus delayed decompression for traumatic cervical spinal cord injury: results of the Surgical Timing in Acute Spinal Cord Injury Study (STASCIS). PLoS ONE 7:e320372012

    • Search Google Scholar
    • Export Citation
  • 31

    Fehlings MGWilson JRFrankowski RFToups EGAarabi BHarrop JS: Riluzole for the treatment of acute traumatic spinal cord injury: rationale for and design of the NACTN Phase I clinical trial. J Neurosurg Spine 17:1 Suppl1511562012

    • Search Google Scholar
    • Export Citation
  • 32

    Fehlings MGWilson JRKaradimas SKArnold PMKopjar B: Clinical evaluation of a neuroprotective drug in patients with cervical spondylotic myelopathy undergoing surgical treatment: design and rationale for the CSM-Protect trial. Spine (Phila Pa 1976) 38:22 Suppl 1S68S752013

    • Search Google Scholar
    • Export Citation
  • 33

    Feng HYNing GZFeng SQYu TQZhou HX: Epidemiological profile of 239 traumatic spinal cord injury cases over a period of 12 years in Tianjin, China. J Spinal Cord Med 34:3883942011

    • Search Google Scholar
    • Export Citation
  • 34

    Flanders AESchaefer DMDoan HTMishkin MMGonzalez CFNorthrup BE: Acute cervical spine trauma: correlation of MR imaging findings with degree of neurologic deficit. Radiology 177:25331990

    • Search Google Scholar
    • Export Citation
  • 35

    Fleming JCNorenberg MDRamsay DADekaban GAMarcillo AESaenz AD: The cellular inflammatory response in human spinal cords after injury. Brain 129:324932692006

    • Search Google Scholar
    • Export Citation
  • 36

    Freund PSchmidlin EWannier TBloch JMir ASchwab ME: Anti-Nogo-A antibody treatment promotes recovery of manual dexterity after unilateral cervical lesion in adult primates—re-examination and extension of behavioral data. Eur J Neurosci 29:9839962009

    • Search Google Scholar
    • Export Citation
  • 37

    Fujii HYone KSakou T: Magnetic resonance imaging study of experimental acute spinal cord injury. Spine (Phila Pa 1976) 18:203020341993

    • Search Google Scholar
    • Export Citation
  • 38

    Furlan JCFehlings MGMassicotte EMAarabi BVaccaro ARBono CM: A quantitative and reproducible method to assess cord compression and canal stenosis after cervical spine trauma: a study of interrater and intrarater reliability. Spine (Phila Pa 1976) 32:208320912007

    • Search Google Scholar
    • Export Citation
  • 39

    Furlan JCKailaya-Vasan AAarabi BFehlings M: A novel approach to quantitatively assess posttraumatic cervical spinal canal compromise and spinal cord compression: a multicenter responsiveness study. Spine (Phila Pa 1976) 36:7847932011

    • Search Google Scholar
    • Export Citation
  • 40

    Furlan JCNoonan VCadotte DWFehlings MG: Timing of decompressive surgery of spinal cord after traumatic spinal cord injury: an evidence-based examination of pre-clinical and clinical studies. J Neurotrauma 28:137113992011

    • Search Google Scholar
    • Export Citation
  • 41

    Guidelines for the management of acute cervical spine and spinal cord injuries. Neurosurgery 50:3 SupplS1S1982002

  • 42

    Guth LZhang ZSteward O: The unique histopathological responses of the injured spinal cord. Implications for neuroprotective therapy. Ann N Y Acad Sci 890:3663841999

    • Search Google Scholar
    • Export Citation
  • 43

    Hovda DABecker DPKatayama Y: Secondary injury and acidosis. J Neurotrauma 9:Suppl 1S47S601992

  • 44

    Hurlbert RJHamilton MG: Methylprednisolone for acute spinal cord injury: 5-year practice reversal. Can J Neurol Sci 35:41452008

  • 45

    Iizuka HYamamoto HIwasaki YYamamoto TKonno H: Evolution of tissue damage in compressive spinal cord injury in rats. J Neurosurg 66:5956031987

    • Search Google Scholar
    • Export Citation
  • 46

    Jimenez OMarcillo ALevi AD: A histopathological analysis of the human cervical spinal cord in patients with acute traumatic central cord syndrome. Spinal Cord 38:5325372000

    • Search Google Scholar
    • Export Citation
  • 47

    Kalsi-Ryan SWilson JYang JMFehlings MG: Neurological grading in traumatic spinal cord injury. World Neurosurg 82:5095182014

  • 48

    Kawata KMorimoto TOhashi TTsujimoto SHoshida TTsunoda S: [Experimental study of acute spinal cord injury: a histopathological study]. No Shinkei Geka 21:45511993. (Jpn)

    • Search Google Scholar
    • Export Citation
  • 49

    Kurland DHong CAarabi BGerzanich VSimard JM: Hemorrhagic progression of a contusion after traumatic brain injury: a review. J Neurotrauma 29:19312012

    • Search Google Scholar
    • Export Citation
  • 50

    Kwon BKFisher CGBoyd MCCobb JJebson HNoonan V: A prospective randomized controlled trial of anterior compared with posterior stabilization for unilateral facet injuries of the cervical spine. J Neurosurg Spine 7:1122007

    • Search Google Scholar
    • Export Citation
  • 51

    Kwon BKTetzlaff WGrauer JNBeiner JVaccaro AR: Pathophysiology and pharmacologic treatment of acute spinal cord injury. Spine J 4:4514642004

    • Search Google Scholar
    • Export Citation
  • 52

    Management of acute spinal cord injuries in an intensive care unit or other monitored setting. Neurosurgery 50:3 SupplS51S572002

  • 53

    Martin DSchoenen JLenelle JReznik MMoonen G: MRI-pathological correlations in acute traumatic central cord syndrome: case report. Neuroradiology 34:2622661992

    • Search Google Scholar
    • Export Citation
  • 54

    Miyanji FFurlan JCAarabi BArnold PMFehlings MG: Acute cervical traumatic spinal cord injury: MR imaging findings correlated with neurologic outcome—prospective study with 100 consecutive patients. Radiology 243:8208272007

    • Search Google Scholar
    • Export Citation
  • 55

    National Spinal Cord Injury Statistical Center: Spinal cord injury facts and figures at a glance. J Spinal Cord Med 37:1171182014

  • 56

    Nishi RALiu HChu YHamamura MSu MYNalcioglu O: Behavioral, histological, and ex vivo magnetic resonance imaging assessment of graded contusion spinal cord injury in mice. J Neurotrauma 24:6746892007

    • Search Google Scholar
    • Export Citation
  • 57

    Nout YSMihai GTovar CASchmalbrock PBresnahan JCBeattie MS: Hypertonic saline attenuates cord swelling and edema in experimental spinal cord injury: a study utilizing magnetic resonance imaging. Crit Care Med 37:216021662009

    • Search Google Scholar
    • Export Citation
  • 58

    Papadopoulos SMSelden NRQuint DJPatel NGillespie BGrube S: Immediate spinal cord decompression for cervical spinal cord injury: feasibility and outcome. J Trauma 52:3233322002

    • Search Google Scholar
    • Export Citation
  • 59

    Quencer RMBunge RPEgnor MGreen BAPuckett WNaidich TP: Acute traumatic central cord syndrome: MRI-pathological correlations. Neuroradiology 34:85941992

    • Search Google Scholar
    • Export Citation
  • 60

    Schaefer DMFlanders ANorthrup BEDoan HTOsterholm JL: Magnetic resonance imaging of acute cervical spine trauma. Correlation with severity of neurologic injury. Spine (Phila Pa 1976) 14:109010951989

    • Search Google Scholar
    • Export Citation
  • 61

    Schaefer DMFlanders AEOsterholm JLNorthrup BE: Prognostic significance of magnetic resonance imaging in the acute phase of cervical spine injury. J Neurosurg 76:2182231992

    • Search Google Scholar
    • Export Citation
  • 62

    Senter HJVenes JL: Loss of autoregulation and posttraumatic ischemia following experimental spinal cord trauma. J Neurosurg 50:1982061979

    • Search Google Scholar
    • Export Citation
  • 63

    Short D: Is the role of steroids in acute spinal cord injury now resolved?. Curr Opin Neurol 14:7597632001

  • 64

    Simard JMPopovich PGTsymbalyuk OCaridi JGullapalli RPKilbourne MJ: MRI evidence that glibenclamide reduces acute lesion expansion in a rat model of spinal cord injury. Spinal Cord 51:8238272013

    • Search Google Scholar
    • Export Citation
  • 65

    Simard JMPopovich PGTsymbalyuk OGerzanich V: Spinal cord injury with unilateral versus bilateral primary hemorrhage—effects of glibenclamide. Exp Neurol 233:8298352012

    • Search Google Scholar
    • Export Citation
  • 66

    Simard JMWoo SKNorenberg MDTosun CChen ZIvanova S: Brief suppression of Abcc8 prevents autodestruction of spinal cord after trauma. Sci Transl Med 2:28ra292010

    • Search Google Scholar
    • Export Citation
  • 67

    Tator CH: Review of experimental spinal cord injury with emphasis on the local and systemic circulatory effects. Neurochirurgie 37:2913021991

    • Search Google Scholar
    • Export Citation
  • 68

    Tator CHFehlings MG: Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms. J Neurosurg 75:15261991

    • Search Google Scholar
    • Export Citation
  • 69

    Turnbull IM: Chapter 5. Blood supply of the spinal cord: normal and pathological considerations. Clin Neurosurg 20:56841973

  • 70

    Turnbull IM: Microvasculature of the human spinal cord. J Neurosurg 35:1411471971

  • 71

    Vaccaro ARDaugherty RJSheehan TPDante SJCotler JMBalderston RA: Neurologic outcome of early versus late surgery for cervical spinal cord injury. Spine (Phila Pa 1976) 22:260926131997

    • Search Google Scholar
    • Export Citation
  • 72

    Vaccaro ARHulbert RJPatel AAFisher CDvorak MLehman RA Jr: The subaxial cervical spine injury classification system: a novel approach to recognize the importance of morphology, neurology, and integrity of the disco-ligamentous complex. Spine (Phila Pa 1976) 32:236523742007

    • Search Google Scholar
    • Export Citation
  • 73

    Vale FLBurns JJackson ABHadley MN: Combined medical and surgical treatment after acute spinal cord injury: results of a prospective pilot study to assess the merits of aggressive medical resuscitation and blood pressure management. J Neurosurg 87:2392461997

    • Search Google Scholar
    • Export Citation
  • 74

    van Middendorp JJHosman AJDoi SA: The effects of the timing of spinal surgery after traumatic spinal cord injury: a systematic review and meta-analysis. J Neurotrauma 30:178117942013

    • Search Google Scholar
    • Export Citation
  • 75

    Wagner FC JrDohrmann GJBucy PC: Histopathology of transitory traumatic paraplegia in the monkey. J Neurosurg 35:2722761971

  • 76

    Waring WP IIIBiering-Sorensen FBurns SDonovan WGraves DJha A: 2009 review and revisions of the International Standards for the Neurological Classification of Spinal Cord Injury. J Spinal Cord Med 33:3463522010

    • Search Google Scholar
    • Export Citation
  • 77

    Wilson JRArnold PMSingh AKalsi-Ryan SFehlings MG: Clinical prediction model for acute inpatient complications after traumatic cervical spinal cord injury: a subanalysis from the Surgical Timing in Acute Spinal Cord Injury Study. J Neurosurg Spine 17:1 Suppl46512012

    • Search Google Scholar
    • Export Citation
  • 78

    Wilson JRFehlings MG: Riluzole for acute traumatic spinal cord injury: a promising neuroprotective treatment strategy. World Neurosurg 81:8258292014

    • Search Google Scholar
    • Export Citation
  • 79

    Wilson JRGrossman RGFrankowski RFKiss ADavis AMKulkarni AV: A clinical prediction model for longterm functional outcome after traumatic spinal cord injury based on acute clinical and imaging factors. J Neurotrauma 29:226322712012

    • Search Google Scholar
    • Export Citation
  • 80

    Wilson JRSingh ACraven CVerrier MCDrew BAhn H: Early versus late surgery for traumatic spinal cord injury: the results of a prospective Canadian cohort study. Spinal Cord 50:8408432012

    • Search Google Scholar
    • Export Citation
  • 81

    Wu YSatkunendrarajah KTeng YChow DSButtigieg JFehlings MG: Delayed post-injury administration of riluzole is neuroprotective in a preclinical rodent model of cervical spinal cord injury. J Neurotrauma 30:4414522013

    • Search Google Scholar
    • Export Citation
  • 82

    Yang RGuo LWang PHuang LTang YWang W: Epidemiology of spinal cord injuries and risk factors for complete injuries in Guangdong, China: a retrospective study. PLoS ONE 9:e847332014

    • Search Google Scholar
    • Export Citation

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Article Information

Contributor Notes

Correspondence Bizhan Aarabi, Department of Neurosurgery, University of Maryland School of Medicine, 22 S. Greene St., Ste. S-12-D, Baltimore, MD 21201. email: baarabi@smail.umaryland.edu.INCLUDE WHEN CITING Published online March 6, 2015; DOI: 10.3171/2014.10.SPINE14576.DISCLOSURE The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.
Headings
Figures
  • View in gallery

    Midsagittal reformatted STIR image obtained 8.5 hours after trauma in a 27-year-old man who was involved in an automobile accident and sustained a C-6 teardrop fracture that resulted in quadriplegia. On admission, his AMS was 27 and his AIS grade was A. He underwent circumferential realignment, decompression, and internal fixation 20 hours after the trauma. The image indicates the Da, Di, Db, da, di, and db, parameters that were used to calculate the MCC and MSCC. The patient continued to have an AMS of 28 and AIS grade of A 11 months after the trauma. See Calculation of Maximum Canal Compromise, Maximum Spinal Cord Compression, and IML expansion Rate for the full explanation.

  • View in gallery

    Scatter plot demonstrating the relationship between the IML expansion rate and the time past injury to the first MRI scan (Interval 1). The expansion rate increases as the MR image acquisition approaches the time of trauma.

  • View in gallery

    Midsagittal reformatted CT and MR images of the cervical spine of a 20-year-old woman admitted to the trauma resuscitation unit after an automobile accident with an AMS of 89 (AIS Grade D). Forty-two months after decompression and circumferential internal fixation, her AMS was 99 and her AIS grade was D. A: Teardrop compression fracture of C-6 (white arrow). B: A lesion 32 mm long with high signal intensity 14.4 hours after the trauma (bracket 1). C: At 64.8 hours after the injury and after decompression, realignment, and internal fixation, her MR image showed a high-intensity signal that was 35.9 mm long (bracket 2). The IML expansion rate in this patient was 80 μm/hour.

  • View in gallery

    Midsagittal preoperative (A and B) and postoperative (C and D) CT and MR images of a 25-year-old man who sustained a traumatic C-5 compression fracture. At the time of admission, his AMS was 12 and his AIS grade was A. Ten months after injury, he remained quadriplegic. Shown are a C-5 teardrop fracture (A) (white arrow), a preoperative MR image 4.5 hours after injury with an intramedullary high-intensity signal measuring 76.2 mm in length (B) (bracket E), a postoperative CT image (C), and a postoperative MR image 44 hours after injury demonstrating an IML measuring 259 mm in length (D) (bracket F). The IML expansion rate was 3200 μm/hour.

  • View in gallery

    Scatter plot illustrating a progressive decline in IML expansion with increased patient age.

  • View in gallery

    Scatter plot demonstrating the relationship between the IML expansion rate and AMS at admission. Lower AMSs tended to have faster IML expansion rates.

  • View in gallery

    Scatter plot depicting the relationship between time to surgery and the IML expansion rate.

  • View in gallery

    Histogram showing the relationship between injury morphology and the IML expansion rate. DISC/OST= disc/osteophyte complex.

  • View in gallery

    Histogram illustrating the relationship between AIS grade and the IML expansion rate.

References
  • 1

    Aarabi BAlexander MMirvis SEShanmuganathan KChesler DMaulucci C: Predictors of outcome in acute traumatic central cord syndrome due to spinal stenosis. J Neurosurg Spine 14:1221302011

    • Search Google Scholar
    • Export Citation
  • 2

    Aarabi BSimard JMKufera JAAlexander MZacherl KMMirvis SE: Intramedullary lesion expansion on magnetic resonance imaging in patients with motor complete cervical spinal cord injury. J Neurosurg Spine 17:2432502012

    • Search Google Scholar
    • Export Citation
  • 3

    Ackery ATator CKrassioukov A: A global perspective on spinal cord injury epidemiology. J Neurotrauma 21:135513702004

  • 4

    Alexander RHProctor HJ: Advanced Trauma Life Support (ATLS) Program for Physicians ChicagoAmerican College of Surgeons1993

  • 5

    Allen AR: Remarks on the histopathological changes in the spinal cord due to impact. An experimental study. J Nerve Ment Dis 41:1411471914

    • Search Google Scholar
    • Export Citation
  • 6

    Allen AR: Surgery of experimental lesion of spinal cord equivalent to crush injury of fracture dislocation of spinal column: a preliminary report. JAMA 57:8788801911

    • Search Google Scholar
    • Export Citation
  • 7

    Allen BL JrFerguson RLLehmann TRO'Brien RP: A mechanistic classification of closed, indirect fractures and dislocations of the lower cervical spine. Spine (Phila Pa 1976) 7:1271982

    • Search Google Scholar
    • Export Citation
  • 8

    Amar APLevy ML: Pathogenesis and pharmacological strategies for mitigating secondary damage in acute spinal cord injury. Neurosurgery 44:102710401999

    • Search Google Scholar
    • Export Citation
  • 9

    American College of Surgeons: Advanced Trauma Life Support (ATLS) ed 7ChicagoAmerican College of Surgeons2004

  • 10

    Anderberg LAldskogius HHoltz A: Spinal cord injury—scientific challenges for the unknown future. Ups J Med Sci 112:2592882007

    • Search Google Scholar
    • Export Citation
  • 11

    Anderson DK: Chemical and cellular mediators in spinal cord injury. J Neurotrauma 9:1431461992

  • 12

    Anthes DLTheriault ETator CH: Ultrastructural evidence for arteriolar vasospasm after spinal cord trauma. Neurosurgery 39:8048141996

    • Search Google Scholar
    • Export Citation
  • 13

    Baptiste DCFehlings MG: Pharmacological approaches to repair the injured spinal cord. J Neurotrauma 23:3183342006

  • 14

    Blood pressure management after acute spinal cord injury. Neurosurgery 50:3 SupplS58S622002

  • 15

    Bracken MBShepard MJHolford TRLeo-Summers LAldrich EFFazl M: Administration of methylprednisolone for 24 or 48 hours or tirilazad mesylate for 48 hours in the treatment of acute spinal cord injury. Results of the Third National Acute Spinal Cord Injury Randomized Controlled Trial. JAMA 277:159716041997

    • Search Google Scholar
    • Export Citation
  • 16

    Buchanan LEDitunno JF JrOsterholm JLCotler JMStaas WE Jr: Spinal cord injury: a ten-year report. Pa Med 93:36391990

  • 17

    Cadotte DWFehlings MG: Spinal cord injury: a systematic review of current treatment options. Clin Orthop Relat Res 469:7327412011

    • Search Google Scholar
    • Export Citation
  • 18

    Carlson GDWarden KEBarbeau JMBahniuk EKutina-Nelson KLBiro CL: Viscoelastic relaxation and regional blood flow response to spinal cord compression and decompression. Spine (Phila Pa 1976) 22:128512911997

    • Search Google Scholar
    • Export Citation
  • 19

    Carlson SLParrish MESpringer JEDoty KDossett L: Acute inflammatory response in spinal cord following impact injury. Exp Neurol 151:77881998

    • Search Google Scholar
    • Export Citation
  • 20

    Chou PCShunmugavel AEl Sayed HDesouki MMNguyen SAKhan M: Preclinical use of longitudinal MRI for screening the efficacy of S-nitrosoglutathione in treating spinal cord injury. J Magn Reson Imaging 33:130113112011

    • Search Google Scholar
    • Export Citation
  • 21

    Chow DSTeng YToups EGAarabi BHarrop JSShaffrey CI: Pharmacology of riluzole in acute spinal cord injury. J Neurosurg Spine 17:1 Suppl1291402012

    • Search Google Scholar
    • Export Citation
  • 22

    Devivo MJ: Epidemiology of traumatic spinal cord injury: trends and future implications. Spinal Cord 50:3653722012

  • 23

    Dohrmann GJWagner FC JrBucy PC: The microvasculature in transitory traumatic paraplegia. An electron microscopic study in the monkey. J Neurosurg 35:2632711971

    • Search Google Scholar
    • Export Citation
  • 24

    Dohrmann GJWagner FC JrBucy PC: Transitory traumatic paraplegia: electron microscopy of early alterations in myelinated nerve fibers. J Neurosurg 36:4074151972

    • Search Google Scholar
    • Export Citation
  • 25

    Dvorak MFFisher CGFehlings MGRampersaud YROner FCAarabi B: The surgical approach to subaxial cervical spine injuries: an evidence-based algorithm based on the SLIC classification system. Spine (Phila Pa 1976) 32:262026292007

    • Search Google Scholar
    • Export Citation
  • 26

    Fairholm DJTurnbull IM: Microangiographic study of experimental spinal cord injuries. J Neurosurg 35:2772861971

  • 27

    Fehlings MGBaptiste DC: Current status of clinical trials for acute spinal cord injury. Injury 36:Suppl 2B113B1222005

  • 28

    Fehlings MGFurlan JCMassicotte EMArnold PAarabi BHarrop J: Interobserver and intraobserver reliability of maximum canal compromise and spinal cord compression for evaluation of acute traumatic cervical spinal cord injury. Spine (Phila Pa 1976) 31:171917252006

    • Search Google Scholar
    • Export Citation
  • 29

    Fehlings MGRao SCTator CHSkaf GArnold PBenzel E: The optimal radiologic method for assessing spinal canal compromise and cord compression in patients with cervical spinal cord injury. Part II: Results of a multicenter study. Spine (Phila Pa 1976) 24:6056131999

    • Search Google Scholar
    • Export Citation
  • 30

    Fehlings MGVaccaro AWilson JRSingh ACadotte WDHarrop JS: Early versus delayed decompression for traumatic cervical spinal cord injury: results of the Surgical Timing in Acute Spinal Cord Injury Study (STASCIS). PLoS ONE 7:e320372012

    • Search Google Scholar
    • Export Citation
  • 31

    Fehlings MGWilson JRFrankowski RFToups EGAarabi BHarrop JS: Riluzole for the treatment of acute traumatic spinal cord injury: rationale for and design of the NACTN Phase I clinical trial. J Neurosurg Spine 17:1 Suppl1511562012

    • Search Google Scholar
    • Export Citation
  • 32

    Fehlings MGWilson JRKaradimas SKArnold PMKopjar B: Clinical evaluation of a neuroprotective drug in patients with cervical spondylotic myelopathy undergoing surgical treatment: design and rationale for the CSM-Protect trial. Spine (Phila Pa 1976) 38:22 Suppl 1S68S752013

    • Search Google Scholar
    • Export Citation
  • 33

    Feng HYNing GZFeng SQYu TQZhou HX: Epidemiological profile of 239 traumatic spinal cord injury cases over a period of 12 years in Tianjin, China. J Spinal Cord Med 34:3883942011

    • Search Google Scholar
    • Export Citation
  • 34

    Flanders AESchaefer DMDoan HTMishkin MMGonzalez CFNorthrup BE: Acute cervical spine trauma: correlation of MR imaging findings with degree of neurologic deficit. Radiology 177:25331990

    • Search Google Scholar
    • Export Citation
  • 35

    Fleming JCNorenberg MDRamsay DADekaban GAMarcillo AESaenz AD: The cellular inflammatory response in human spinal cords after injury. Brain 129:324932692006

    • Search Google Scholar
    • Export Citation
  • 36

    Freund PSchmidlin EWannier TBloch JMir ASchwab ME: Anti-Nogo-A antibody treatment promotes recovery of manual dexterity after unilateral cervical lesion in adult primates—re-examination and extension of behavioral data. Eur J Neurosci 29:9839962009

    • Search Google Scholar
    • Export Citation
  • 37

    Fujii HYone KSakou T: Magnetic resonance imaging study of experimental acute spinal cord injury. Spine (Phila Pa 1976) 18:203020341993

    • Search Google Scholar
    • Export Citation
  • 38

    Furlan JCFehlings MGMassicotte EMAarabi BVaccaro ARBono CM: A quantitative and reproducible method to assess cord compression and canal stenosis after cervical spine trauma: a study of interrater and intrarater reliability. Spine (Phila Pa 1976) 32:208320912007

    • Search Google Scholar
    • Export Citation
  • 39

    Furlan JCKailaya-Vasan AAarabi BFehlings M: A novel approach to quantitatively assess posttraumatic cervical spinal canal compromise and spinal cord compression: a multicenter responsiveness study. Spine (Phila Pa 1976) 36:7847932011

    • Search Google Scholar
    • Export Citation
  • 40

    Furlan JCNoonan VCadotte DWFehlings MG: Timing of decompressive surgery of spinal cord after traumatic spinal cord injury: an evidence-based examination of pre-clinical and clinical studies. J Neurotrauma 28:137113992011

    • Search Google Scholar
    • Export Citation
  • 41

    Guidelines for the management of acute cervical spine and spinal cord injuries. Neurosurgery 50:3 SupplS1S1982002

  • 42

    Guth LZhang ZSteward O: The unique histopathological responses of the injured spinal cord. Implications for neuroprotective therapy. Ann N Y Acad Sci 890:3663841999

    • Search Google Scholar
    • Export Citation
  • 43

    Hovda DABecker DPKatayama Y: Secondary injury and acidosis. J Neurotrauma 9:Suppl 1S47S601992

  • 44

    Hurlbert RJHamilton MG: Methylprednisolone for acute spinal cord injury: 5-year practice reversal. Can J Neurol Sci 35:41452008

  • 45

    Iizuka HYamamoto HIwasaki YYamamoto TKonno H: Evolution of tissue damage in compressive spinal cord injury in rats. J Neurosurg 66:5956031987

    • Search Google Scholar
    • Export Citation
  • 46

    Jimenez OMarcillo ALevi AD: A histopathological analysis of the human cervical spinal cord in patients with acute traumatic central cord syndrome. Spinal Cord 38:5325372000

    • Search Google Scholar
    • Export Citation
  • 47

    Kalsi-Ryan SWilson JYang JMFehlings MG: Neurological grading in traumatic spinal cord injury. World Neurosurg 82:5095182014

  • 48

    Kawata KMorimoto TOhashi TTsujimoto SHoshida TTsunoda S: [Experimental study of acute spinal cord injury: a histopathological study]. No Shinkei Geka 21:45511993. (Jpn)

    • Search Google Scholar
    • Export Citation
  • 49

    Kurland DHong CAarabi BGerzanich VSimard JM: Hemorrhagic progression of a contusion after traumatic brain injury: a review. J Neurotrauma 29:19312012

    • Search Google Scholar
    • Export Citation
  • 50

    Kwon BKFisher CGBoyd MCCobb JJebson HNoonan V: A prospective randomized controlled trial of anterior compared with posterior stabilization for unilateral facet injuries of the cervical spine. J Neurosurg Spine 7:1122007

    • Search Google Scholar
    • Export Citation
  • 51

    Kwon BKTetzlaff WGrauer JNBeiner JVaccaro AR: Pathophysiology and pharmacologic treatment of acute spinal cord injury. Spine J 4:4514642004

    • Search Google Scholar
    • Export Citation
  • 52

    Management of acute spinal cord injuries in an intensive care unit or other monitored setting. Neurosurgery 50:3 SupplS51S572002

  • 53

    Martin DSchoenen JLenelle JReznik MMoonen G: MRI-pathological correlations in acute traumatic central cord syndrome: case report. Neuroradiology 34:2622661992

    • Search Google Scholar
    • Export Citation
  • 54

    Miyanji FFurlan JCAarabi BArnold PMFehlings MG: Acute cervical traumatic spinal cord injury: MR imaging findings correlated with neurologic outcome—prospective study with 100 consecutive patients. Radiology 243:8208272007

    • Search Google Scholar
    • Export Citation
  • 55

    National Spinal Cord Injury Statistical Center: Spinal cord injury facts and figures at a glance. J Spinal Cord Med 37:1171182014

  • 56

    Nishi RALiu HChu YHamamura MSu MYNalcioglu O: Behavioral, histological, and ex vivo magnetic resonance imaging assessment of graded contusion spinal cord injury in mice. J Neurotrauma 24:6746892007

    • Search Google Scholar
    • Export Citation
  • 57

    Nout YSMihai GTovar CASchmalbrock PBresnahan JCBeattie MS: Hypertonic saline attenuates cord swelling and edema in experimental spinal cord injury: a study utilizing magnetic resonance imaging. Crit Care Med 37:216021662009

    • Search Google Scholar
    • Export Citation
  • 58

    Papadopoulos SMSelden NRQuint DJPatel NGillespie BGrube S: Immediate spinal cord decompression for cervical spinal cord injury: feasibility and outcome. J Trauma 52:3233322002

    • Search Google Scholar
    • Export Citation
  • 59

    Quencer RMBunge RPEgnor MGreen BAPuckett WNaidich TP: Acute traumatic central cord syndrome: MRI-pathological correlations. Neuroradiology 34:85941992

    • Search Google Scholar
    • Export Citation
  • 60

    Schaefer DMFlanders ANorthrup BEDoan HTOsterholm JL: Magnetic resonance imaging of acute cervical spine trauma. Correlation with severity of neurologic injury. Spine (Phila Pa 1976) 14:109010951989

    • Search Google Scholar
    • Export Citation
  • 61

    Schaefer DMFlanders AEOsterholm JLNorthrup BE: Prognostic significance of magnetic resonance imaging in the acute phase of cervical spine injury. J Neurosurg 76:2182231992

    • Search Google Scholar
    • Export Citation
  • 62

    Senter HJVenes JL: Loss of autoregulation and posttraumatic ischemia following experimental spinal cord trauma. J Neurosurg 50:1982061979

    • Search Google Scholar
    • Export Citation
  • 63

    Short D: Is the role of steroids in acute spinal cord injury now resolved?. Curr Opin Neurol 14:7597632001

  • 64

    Simard JMPopovich PGTsymbalyuk OCaridi JGullapalli RPKilbourne MJ: MRI evidence that glibenclamide reduces acute lesion expansion in a rat model of spinal cord injury. Spinal Cord 51:8238272013

    • Search Google Scholar
    • Export Citation
  • 65

    Simard JMPopovich PGTsymbalyuk OGerzanich V: Spinal cord injury with unilateral versus bilateral primary hemorrhage—effects of glibenclamide. Exp Neurol 233:8298352012

    • Search Google Scholar
    • Export Citation
  • 66

    Simard JMWoo SKNorenberg MDTosun CChen ZIvanova S: Brief suppression of Abcc8 prevents autodestruction of spinal cord after trauma. Sci Transl Med 2:28ra292010

    • Search Google Scholar
    • Export Citation
  • 67

    Tator CH: Review of experimental spinal cord injury with emphasis on the local and systemic circulatory effects. Neurochirurgie 37:2913021991

    • Search Google Scholar
    • Export Citation
  • 68

    Tator CHFehlings MG: Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms. J Neurosurg 75:15261991

    • Search Google Scholar
    • Export Citation
  • 69

    Turnbull IM: Chapter 5. Blood supply of the spinal cord: normal and pathological considerations. Clin Neurosurg 20:56841973

  • 70

    Turnbull IM: Microvasculature of the human spinal cord. J Neurosurg 35:1411471971

  • 71

    Vaccaro ARDaugherty RJSheehan TPDante SJCotler JMBalderston RA: Neurologic outcome of early versus late surgery for cervical spinal cord injury. Spine (Phila Pa 1976) 22:260926131997

    • Search Google Scholar
    • Export Citation
  • 72

    Vaccaro ARHulbert RJPatel AAFisher CDvorak MLehman RA Jr: The subaxial cervical spine injury classification system: a novel approach to recognize the importance of morphology, neurology, and integrity of the disco-ligamentous complex. Spine (Phila Pa 1976) 32:236523742007

    • Search Google Scholar
    • Export Citation
  • 73

    Vale FLBurns JJackson ABHadley MN: Combined medical and surgical treatment after acute spinal cord injury: results of a prospective pilot study to assess the merits of aggressive medical resuscitation and blood pressure management. J Neurosurg 87:2392461997

    • Search Google Scholar
    • Export Citation
  • 74

    van Middendorp JJHosman AJDoi SA: The effects of the timing of spinal surgery after traumatic spinal cord injury: a systematic review and meta-analysis. J Neurotrauma 30:178117942013

    • Search Google Scholar
    • Export Citation
  • 75

    Wagner FC JrDohrmann GJBucy PC: Histopathology of transitory traumatic paraplegia in the monkey. J Neurosurg 35:2722761971

  • 76

    Waring WP IIIBiering-Sorensen FBurns SDonovan WGraves DJha A: 2009 review and revisions of the International Standards for the Neurological Classification of Spinal Cord Injury. J Spinal Cord Med 33:3463522010

    • Search Google Scholar
    • Export Citation
  • 77

    Wilson JRArnold PMSingh AKalsi-Ryan SFehlings MG: Clinical prediction model for acute inpatient complications after traumatic cervical spinal cord injury: a subanalysis from the Surgical Timing in Acute Spinal Cord Injury Study. J Neurosurg Spine 17:1 Suppl46512012

    • Search Google Scholar
    • Export Citation
  • 78

    Wilson JRFehlings MG: Riluzole for acute traumatic spinal cord injury: a promising neuroprotective treatment strategy. World Neurosurg 81:8258292014

    • Search Google Scholar
    • Export Citation
  • 79

    Wilson JRGrossman RGFrankowski RFKiss ADavis AMKulkarni AV: A clinical prediction model for longterm functional outcome after traumatic spinal cord injury based on acute clinical and imaging factors. J Neurotrauma 29:226322712012

    • Search Google Scholar
    • Export Citation
  • 80

    Wilson JRSingh ACraven CVerrier MCDrew BAhn H: Early versus late surgery for traumatic spinal cord injury: the results of a prospective Canadian cohort study. Spinal Cord 50:8408432012

    • Search Google Scholar
    • Export Citation
  • 81

    Wu YSatkunendrarajah KTeng YChow DSButtigieg JFehlings MG: Delayed post-injury administration of riluzole is neuroprotective in a preclinical rodent model of cervical spinal cord injury. J Neurotrauma 30:4414522013

    • Search Google Scholar
    • Export Citation
  • 82

    Yang RGuo LWang PHuang LTang YWang W: Epidemiology of spinal cord injuries and risk factors for complete injuries in Guangdong, China: a retrospective study. PLoS ONE 9:e847332014

    • Search Google Scholar
    • Export Citation
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