ORIGINAL ARTICLE

Spinal cord injury without radiologic abnormality in children imaged with magnetic resonance imaging Prashant Mahajan, MD, MPH, MBA, David M. Jaffe, MD, Cody S. Olsen, MS, Jeffrey R. Leonard, MD, Lise E. Nigrovic, MD, MPH, Alexander J. Rogers, MD, Nathan Kuppermann, MD, MPH, and Julie C. Leonard, MD, MPH, Detroit, Michigan

This study aimed to compare children diagnosed with cervical spinal cord injury without radiographic abnormality (SCIWORA) relative to whether there is evidence of cervical spinal cord abnormalities on magnetic resonance imaging (MRI). METHODS: We conducted a planned subanalysis of a cohort of children younger than 16 years with blunt cervical spine injury presenting to Pediatric Emergency Care Applied Research Network centers from January 2000 to December 2004 who underwent cervical MRI and did not have bony or ligamentous injury identified on neuroimaging. We defined SCIWORA with normal MRI finding as children with clinical evidence of cervical cord injury and a normal MRI finding and compared them with children with SCIWORA who had cervical cord signal changes on MRI (abnormal MRI finding). RESULTS: Of the children diagnosed with cervical spine injury, 55% (297 of 540) were imaged with MRI; 69 had no bony or ligamentous injuries and were diagnosed with SCIWORA by clinical evaluation; 54 (78%) had normal MRI finding, and 15 (22%) had cervical cord signal changes on MRI (abnormal MRI finding). Children with abnormal MRI findings were more likely to receive operative stabilization (0% normal MRI finding vs. 20% abnormal MRI finding) and have persistent neurologic deficits at initial hospital discharge (6% normal MRI finding vs. 67% abnormal MRI finding). CONCLUSION: Children diagnosed with SCIWORA but with normal MRI finding in our cohort presented differently and had substantially more favorable clinical outcomes than those with cervical cord abnormalities on MRI. (J Trauma Acute Care Surg. 2013;75: 843Y847. Copyright * 2013 by Lippincott Williams & Wilkins) LEVEL OF EVIDENCE: Epidemiologic study, level III. KEY WORDS: Spinal cord; emergency medicine; radiology; MRI; pediatric. BACKGROUND:

A

lthough spinal cord injuries are uncommon in children, they are associated with severe morbidity for those affected. Children are anatomically predisposed to specific types of spinal cord injuries because of their large head-to-trunk ratio, relatively weak nuchal musculature, anterior wedging of the vertebral bodies, and horizontally oriented facets.1,2 Spinal cord injury without any radiographic abnormality (SCIWORA) is one type of injury thought to be more common in pediatric patients. The diagnosis of SCIWORA is assigned to

Submitted: May 21, 2013, Revised: July 8, 2013, Accepted: July 11, 2013. From the Division of Emergency Medicine (P.M.), Department of Pediatrics, Children’s Hospital of Michigan and Wayne State University School of Medicine, Detroit; and Departments of Emergency Medicine (A.J.R.) and Pediatrics (A.J.R.), University of Michigan Medical Center and University of Michigan School of Medicine, Ann Arbor, Michigan; Department of Pediatrics (D.M.J., J.C.L.), St. Louis Children’s Hospital (D.M.J., J.R.L., J.C.L.) and Washington University School of Medicine, St. Louis, Missouri; Department of Pediatrics (C.S.O.), University of Utah School of Medicine, Salt Lake City, Utah; Department of Neurosurgery (J.R.L.), Division of Emergency Medicine (L.E.N.), Boston Children’s Hospital and Harvard Medical School, Boston, Massachusetts; Departments of Emergency Medicine (N.K.) and Pediatrics(N.K.), University of California, Davis, School of Medicine, Davis, California. This study was presented in part at the AAP National Conference and Exhibition, October 2010, in San Francisco, California. Please see Mahajan PV, Jaffe DM, Olsen CS, Leonard J Nigrovic LE, Rogers AJ, Kuppermann N, Leonard J, for the PECARN C-Spine Study Group. Spinal cord injury without radiologic abnormality (SCIWORA) in magnetic resonance imaging (MRI) era. Pediatr Emerg Care. 2010;26:697. Address for reprints: Prashant Mahajan, MD, MPH, MBA, Children’s Hospital of Michigan 3901 Beaubien Blvd, Detroit, MI 48201; email: [email protected]. DOI: 10.1097/TA.0b013e3182a74abd

patients with evidence of neurologic deficits attributable to the cervical spinal cord on clinical examination in the absence of overt abnormalities on radiographs or computed tomographic (CT) scans.1 The widespread availability of magnetic resonance imaging (MRI) has substantially altered the evaluation and management of spinal cord injuries including SCIWORA. Indeed, previously undetectable lesions on radiographs or CT scans can now be reclassified based on MRI findings.1,3 This has led some experts to question the clinical relevance of the term SCIWORA and suggest that this condition be redefined in the era of widespread MRI.2,3 We conducted a planned secondary analysis of a retrospective cohort of cervical spineYinjured children with normal conventional radiograph and/or CT scan results at hospital emergency departments (EDs) participating in the Pediatric Emergency Care Applied Research Network (PECARN). We sought to compare the characteristics, presenting symptoms, and clinical outcomes for children with SCIWORA with and without evidence of cervical cord signal changes on MRI.

PATIENTS AND METHODS We conducted a planned secondary analysis of the parent retrospective case-control study of children younger than 16 years with blunt traumaYrelated cervical spine injury who were evaluated and managed at 1 of 17 EDs participating in PECARN between 2000 and 2004. Details of the study design have been described previously.4 The institutional review board

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at each participating center and the PECARN data center approved the study protocol. For this analysis, we identified children with clinical evidence of cervical spinal cord injury who had MRI performed, which along with conventional radiographs and/or cervical spine CT scans (if performed), demonstrated no bony or ligamentous injuries. These patients meet Pang’s definition of SCIWORA.1 Patients were further classified as either having cervical cord signal changes on MRI (abnormal MRI finding) or no cervical cord signal changes on MRI (normal MRI finding) based on imaging findings. For those children who had normal MRI findings, the diagnosis of cervical cord injury was established by either a subspecialist (pediatric orthopedic surgeon or pediatric neurosurgeon) or by the treating physician in those instances where documentation by a subspecialist was not available. The study neurosurgeon (J.R.L.) and principal investigator (J.C.L.) reviewed the case histories, consultant reports, and imaging reports for study patients and confirmed the assigned diagnoses. We excluded children for the following reasons: transfer away from study site ED for definitive care, discharge home from the study site ED, penetrating cervical spine trauma, or insufficient patient information to accurately assess for cervical spine injury. We compared the clinical characteristics, injury mechanisms, and clinical outcomes of patients with normal MRI findings with those with abnormal MRI finding using frequency distributions and Fisher’s exact tests of homogeneity. We used SAS/STAT software for all analyses (version 9.2, SAS Institute Inc., Cary, NC).5 We defined altered mental status as Glasgow Coma Scale (GCS) score less than 15, or Alert, Voice, Pain, Unresponsive (AVPU) scale lower than A or other mental status descriptions deemed by a consensus panel to represent altered level of consciousness. For neurologic outcome, we defined persistent neurologic deficits as any loss or change in sensation, motor loss, muscle weakness, or change in cognitive function that was evident at patient discharge from the study site ED.

RESULTS The parent PECARN cervical spine study included 540 children younger than 16 years with nonpenetrating cervical spine injuries. For this study, 69 children with SCIWORA (13% of overall injured cohort) were included in the analysis. Of these, 54 (78%) had no cervical cord signal changes on MRI (normal MRI finding), while 15 (22%) had cervical cord signal changes on MRI (abnormal MRI finding) (Fig. 1). We excluded 243 (45%) who did not have a spinal MRI performed or did not have results available for review. Within this group, we excluded nine children with a clinical diagnosis of SCIWORA because of nonavailability of MRI results. A detailed review of the medical records of the eight excluded SCIWORA patients with normal MRI finding and single patient with an abnormal MRI finding revealed that none of them required a surgical intervention and they all had normal neurologic outcomes. We compared the demographics, injury mechanisms, and clinical presentations of children with SCIWORA who had normal MRI finding with those who had abnormal MRI finding. Median age was 12 years (interquartile range, 10Y14) 844

Figure 1. Flow chart for included and excluded patients.

for the 54 children with normal MRI finding and 8 years of age (interquartile range, 3Y14) for those with abnormal MRI finding. The majority of patients were male (78% normal MRI finding, 73% abnormal MRI finding) and white (67% normal MRI finding, 60% abnormal MRI finding). For the 15 with abnormal MRI finding, the highest levels of cord injury were at C1 (n = 5), C2 (n = 5), C3 (n = 3), and C5 (n = 2). Injury mechanism differed by injury type (Table 1). Patients with normal MRI finding were more likely than those with abnormal MRI finding to have sports-related mechanisms compared with motor vehicle collision. On clinical evaluation, patients with normal MRI finding were more likely to complain of neck pain and less likely to have an altered mental status at presentation compared with patients with abnormal MRI finding. Cervical spine stabilization methods for SCIWORA differed between the groups with normal MRI and abnormal MRI findings. While all children in the group with normal MRI finding were managed nonoperatively, 20% of children with abnormal MRI finding underwent operative stabilization. In addition, 20% of children in the group with normal MRI finding were discharged without any form of cervical stabilization compared with only 7% of children in the group with abnormal MRI finding (Table 2). Disposition from the ED differed between the two patient groups. Patients with normal MRI finding were less likely to be transferred to the operating room or intensive care unit compared with those with abnormal MRI findings. Children with SCIWORA in the group with normal MRI finding were less likely to have persistent neurologic deficits at discharge from the hospital compared with those with abnormal MRI finding (Table 2). Among children with neurologic deficits, the most common deficit was impaired mobility (cervical cord injury on MRI, 7 of 10 with a persistent deficit, and no cervical cord injury on MRI, 3 of 3 with persistent deficit). Of the 10 children with persistent deficits and abnormal MRI finding, 2 had cognitive impairment at discharge. Our study has several limitations. First, we performed a retrospective study of all children with a site-assigned diagnosis of SCIWORA to identify clinical factors that were abstracted from the medical record review. To limit bias in the chart abstraction process, we created a comprehensive manual * 2013 Lippincott Williams & Wilkins

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TABLE 1. Mechanisms of Injury and Clinical Presentations of Children With SCIWORA and Normal or Abnormal Cervical Cord on MRI SCIWORA and SCIWORA and Normal MRI Abnormal MRI Finding Finding Characteristic ( p*) Mechanism of injury (G0.01) Motor vehicle collision related Fall Dive Sports Other Clinical finding on presentation History of loss of consciousness (1.00) Altered mental status (G0.01) Complaint of neck pain (0.01) Any neck tenderness (G0.01) Torticollis (1.00) Paresthesias (0.14) Sensory loss (0.02) Motor weakness (0.40) Other neurologic deficits (0.10)

n = 54**

n = 15**

3 (6%) 11 (20%) 3 (6%) 27 (50%) 10 (19%)

5 (33%) 7 (47%) 0 (0%) 0 (0%) 3 (20%)

14 (27%) 2 (4%) 29 (56%) 32 (62%) 0 (0%) 27 (53%) 27 (51%) 32 (59%) 5 (9%)

4 (29%) 7 (47%) 2 (14%) 2 (13%) 0 (0%) 4 (29%) 2 (14%) 7 (47%) 4 (27%)

*Fisher’s exact test of homogeneity p value. **Unknown (missing) values were excluded from calculations of percentages. Groups are compared using exact odds ratio estimates and 95% confidence intervals.

of operations and data source hierarchy along with strict study definitions. Data quality was closely monitored by the data coordinating center. Second, SCIWORA case definition may not have been applied consistently owing to missing clinical data. However, we required that all study patients in this subanalysis have a spinal MRI performed, and case classifications were reviewed by a single study neurosurgeon, thus reducing a potential overestimation of SCIWORA prevalence. Third, patients at different medical centers during the study period likely had varying qualities of MRIs performed. Some spinal cord injuries could potentially be reclassified with the availability of higher-quality MRI imaging technology. Lastly, our study sites included local and regional trauma centers with a large number of transferred patients. Therefore, the generalizability of our findings may be limited in nontrauma centers. Nonetheless, the 17 centers that participated in this large study are geographically diverse and represent the spectrum of cervical spine injury seen in children.

DISCUSSION We describe a large multicenter retrospective cohort of children without bony or ligamentous injury to the cervical spine but with evidence of cervical spinal cord injury on physical examination and/or MRI. These children would be variably assigned SCIWORA diagnosis based on previous literature. Clinicians in participating PECARN hospitals applied the term SCIWORA inconsistently to injured children, including the use of terms such as possible, probable, questionable, mild, transient, and sensory SCIWORA. We demonstrated that

children with clinical evidence of cervical cord injury in the presence of a normal MRI finding are different from children with no cervical cord signal changes on MRI in terms of mechanism of injury, clinical presentation, need for surgical intervention, ED disposition, and persistent neurologic deficits at hospital discharge. The initial description of SCIWORA by Pang predates routine MRI for the evaluation of cervical spine injury.6 Since this original work, numerous articles on SCIWORA have been published; however, its epidemiology remains unclear and there is no consensus regarding the definition, demographics, etiology, treatment or prognosis of SCIWORA.2,3 MRI has become a common imaging modality in spinal trauma because of its superior ability to identify soft tissues lesions such as discoligamentous injuries, cord hematomas, cord edema, cord transections, and neurocompressive injuries, which are not evident on radiographs and CT scans.7Y15 It has been suggested that the specialty of the practicing clinician affects the frequency of the diagnosis of SCIWORA with pediatricians, pediatric surgeons, and ED physicians reporting higher incidence rates of this diagnosis compared with orthopedic surgeons and neurosurgeons.3 Previous studies of children with cervical spine injuries have reported a SCIWORA prevalence between 4% and 67%.16Y18 This wide range of reported prevalence is caused by variability in populations studied but more likely owing to the great disparities in the SCIWORA case definition.2,3,19,20 In addition, the prevalence may be overestimated in some series owing to misclassification bias when neurologic deficits are transient and spinal cord injury is not substantiated by MRI. Patients with these clinical findings may have alternative explanations such as brachial plexus, nerve root, or peripheral

TABLE 2. Interventions and Outcomes for Children with SCIWORA With Normal or Abnormal Cervical Cord on MRI SCIWORA and SCIWORA and Normal MRI Abnormal MRI Finding Finding Intervention/Outcome (p*) Glucocorticoids (0.02) Cervical stabilization (0.01) None Nonoperative: cervical collar or brace Operative: halo or internal fixation Disposition (G0.01) Admitted: floor or short stay Admitted: operating room or intensive care unit Neurologic outcome (G0.01) Normal Persistent neurologic deficit Severe cognitive disability Dependent ambulation, wheelchair dependent, or immobile Death during hospitalization

n = 54

n = 15

37 (69%)

5 (33%)

11 (20%) 43 (80%) 0 (0%)

1 (7%) 11 (73%) 3 (20%)

41 (76%) 13 (24%)

3 (20%) 12 (80%)

51 (94%) 3 (6%) 0 3

4 (27%) 10 (67%) 2 7

0 (0%)

1 (7%)

*Fisher’s exact test of homogeneity p value. Groups are compared using exact odds ratio estimates and 95% confidence intervals.

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nerve injuries.2,3,20 To reduce the risk of misclassification bias in our own study, we restricted our analysis to patients who had MRIs performed, and we excluded those children with a site diagnosis of SCIWORA who were discharged from the ED who likely had transient neurologic deficits. A large, multicentered prospective observational study, the National Emergency X-Radiography Utilization Study (NEXUS), included 30 children with cervical spine injury, none of whom had SCIWORA (defined as evidence of spinal cord injury on MRI in the presence of a normal cervical spinal radiograph and CT scan findings when performed).20 The absence of any cases of SCIWORA in this pediatric cohort led the authors to conclude that this condition may not be as common as previously described. It should be noted that we analyzed children with and without cervical cord signal changes on MRI because both groups in previous literature have been diagnosed as SCIWORA, while the NEXUS study assigned SCIWORA diagnosis only to those children who had cervical cord injury on MRI. Despite the differences in definitions of SCIWORA, we similarly found that patients with normal MRI findings have better neurologic outcomes compared with those with evidence of cervical cord signal changes on MRI (abnormal MRI finding). The etiology of SCIWORA as reported in the literature varies by age.1 Motor vehicle collisions, falls, and child abuse are more common mechanisms of injury for children younger than 8 years diagnosed with SCIWORA. Sports-related injuries (gymnastics, diving, horseback riding, American football, and wrestling) are more common mechanisms in older children. Previous reports have identified sports-related injuries21 and falls22 as the commonly associated injury mechanisms. In our cohort, sports-related SCIWORA was more likely associated with normal MRI finding and motor vehicular collisions with abnormal MRI finding. Some children with clinical evidence of persistent neurologic deficits will have normal spine MRI scan findings.1,23,24 In our study, 3 (23%) of the 13 patients with persistent neurologic deficits had normal MRI scan findings. Newer MRI technology such as diffusion-weighted imaging was not routinely clinically available or used during the study period. Looking ahead, advancements in MRI technology may increase the sensitivity for detection of subtle spinal cord injuries, especially in those patients with persistent neurologic deficits. This further highlights the need for redefining spinal cord injury syndromes as technology advances, especially in children.25 Our work clearly identifies two separate groups of children presenting to the ED with neurologic deficits attributable to the cervical spinal cord, those with and those without MRI evidence of cervical cord injury, which under current CSI taxonomy would both be labeled as SCIWORA. These groups differ greatly in presentation, medical management, and ultimate neurologic outcome. Our study findings support the reported evidence that there is indeed a clinical syndrome where persistent cervical myelopathy is present in the face of normal conventional radiograph, CT, and MRI scan findings. Patients in this category should be labeled as SCIWORA or SCIWONA (spinal cord injury without neuroimaging abnormality).26 These patients are more likely to have complete or near-complete neurologic recovery and are unlikely to require operative neurosurgical intervention. Conversely, patients with 846

cervical myelopathy and normal conventional radiograph and/or CT scan finding, but abnormal MRI scan finding, should not be labeled as SCIWORA. They are best described and managed based on the extent of injury on the neural and extraneural structures. Patients in this category have been previously assigned terms such as SCIWOPRA (spinal cord injury without plain radiographic abnormality) and SCIWORET (spinal cord injury without radiologic evidence of trauma).26 This adds further confusion to the taxonomy. We support the recommendations suggested by multiple specialists (pediatrics, neurology, orthopedics, neurosurgery) to standardize spinal cord injury taxonomy.2,3 In this large, multicentered cohort of children with cervical spine injury, we were able to describe children without bony or ligamentous injury but with neurologic deficits referable to the cervical spinal cord. Among these children, those diagnosed clinically with cervical cord injury (SCIWORA with no cervical cord signal changes on MRI) almost uniformly had complete neurologic recovery, and none received operative neurosurgical management. In contrast, those children diagnosed with cervical cord signal changes on MRI had poorer outcomes; some required operative intervention, and a substantial number had persistent neurologic deficits. We suggest that the term SCIWORA be restricted to those patients with evidence of neurologic deficits attributable to the cervical spinal cord and who have normal cervical spine imaging result including MRI. Clear clinical definitions will allow better prognostication, treatment, and epidemiology reporting. We support the recommendation for a multidisciplinary consensus conference2,3 to standardize spinal cord injury taxonomy.

AUTHORSHIP P.M. drafted the manuscript, conducted data analysis, interpreted the data, reviewed and revised the manuscript, and approved the final manuscript as submitted. D.M.J. reviewed and revised the manuscript and approved the final manuscript as submitted. C.S.O. conducted the data analysis, interpreted the data, revised the manuscript, and approved the final manuscript as submitted. J.R.L. reviewed the manuscript, categorized the CSI, and approved the final manuscript as submitted. L.E.N. revised the manuscript and approved the final manuscript as submitted. A.J.R. interpreted the data, revised the manuscript, and approved the final manuscript as submitted. N.K. reviewed and revised the manuscript and approved the final manuscript as submitted. J.C.L. interpreted the data, revised the manuscript, and approved the final manuscript as submitted.

ACKNOWLEDGMENT Participating centers and investigators are listed in the following in alphabetical order: 1. Boston Children’s Hospital, Boston, MA: Lise E. Nigrovic, MD, MPH 2. State University of New York, Buffalo, Buffalo, NY: Kathleen Lillis, MD 3. Children’s Hospital of Michigan, Detroit, MI: Curt Stankovic, MD 4. Children’s Hospital of Philadelphia, Philadelphia, PA: Aaron Donoghue, MD, MSCE 5. Children’s National Medical Center, Washington, DC: Kathleen Brown, MD 6. Cincinnati Children’s Hospital Medical Center, Cincinnati, OH: Scott D. Reeves, MD 7. DeVos Children’s Hospital/Spectrum Health, Grand Rapids, MI: John D. Hoyle, Jr., MD 8. Hurley Medical Center, Flint, MI: Dominic Borgialli, DO, MPH

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9. Johns Hopkins Medical Center, Baltimore, MD: Jennifer Anders, MD 10. Children’s Hospital of Wisconsin, Milwaukee, WI: Greg Rebella, MD 11. Children’s Memorial Hospital, Chicago, IL: Elizabeth Powell, MD 12. Primary Children’s Medical Center, Salt Lake City, UT: Kathleen Adelgais, MD 13. University of California Davis Medical Center, Sacramento, CA: Nathan Kuppermann, MD, MPH, Emily Kim, MPH 14. University of Michigan, Ann Arbor, MI: Alexander J. Rogers, MD 15. University of Rochester Medical Center, Rochester, NY: Lynn Cimpello, MD, MPH 16. University of Maryland, Baltimore, MD: Getachew Teshome, MD, MPH 17. St. Louis Children’s Hospital, St. Louis, MO: Julie C. Leonard, MD, MPH, David M. Jaffe, MD, Jeffrey R. Leonard, MD The C-spine working group for the PECARN network. PECARN Steering Committee: N. Kuppermann, chair; E. Alpern, D. Borgialli, K. Brown, J. Chamberlain, J.M. Dean, G. Foltin, M. Gerardi, M. Gorelick, J. Hoyle, D. Jaffe, C. Johns, K. Lillis, P. Mahajan, R. Maio, S. Miller (deceased), D. Monroe, R. Ruddy, R. Stanley, M. Tunik, A. Walker. MCHB/EMSC liaisons: D. Kavanaugh, H. Park. Central Data Management and Coordinating Center (CDMCC), University of Utah: J.M. Dean, A. Donaldson, R. Holubkov, S. Knight, C. Olsen, S. Zuspan. Feasibility and Budget Subcommittee (FABS): T. Singh, chair; A. Drongowski, L. Fukushima, M. Shults, J. Suhajda, M. Tunik, S. Zuspan. Grants and Publications Subcommittee (GAPS): M. Gorelick, chair; E. Alpern, G. Foltin, R. Holubov, J. Joseph, S. Miller (deceased), F. Moler, O. Soldes, S. Teach. Protocol Concept Review and Development Subcommittee (PCRADS): D. Jaffe, chair; A. Cooper, J. M. Dean, C. Johns, R. Kanter, R. Maio, N.C. Mann, D. Monroe, K. Shaw, D. Treloar. Quality Assurance Subcommittee (QAS): R. Stanley, chair; D. Alexander, J, Burr, M. Gerardi, R. Holubkov, K. Lillis, R. Ruddy, M. Shults, A. Walker Safety and Regulatory Affairs Subcommittee (SRAS): W. Schalick, chair; J. Brennan, J. Burr, J. M. Dean, J. Hoyle, R. Ruddy, T. Singh, D. Snowdon, J. Wright We thank the site PIs and research coordinators in PECARN, whose dedication and hard work made this study possible. DISCLOSURE This study was supported by a grant from the Health Resources and Services Administration/Maternal and Child Health Bureau (HRSA/ MCHB), Division of Research, Education, and Training (DRTE) and the Emergency Medical Services of Children (EMSC) Program (H34 MC04372). The Pediatric Emergency Care Applied Research Network (PECARN) is supported by cooperative agreements U03MC00001, U03MC00003, U03MC00006, U03MC00007, and U03MC00008 from the Emergency Medical Services for Children (EMSC) program of the Maternal and Child Health Bureau, Health Resources and Services Administration, US Department of Health and Human Services.

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Spinal cord injury without radiologic abnormality in children imaged with magnetic resonance imaging.

This study aimed to compare children diagnosed with cervical spinal cord injury without radiographic abnormality (SCIWORA) relative to whether there i...
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