SYSTEMATIC REVIEW

Spinal cord injury without radiologic abnormality in children: A systematic review and meta-analysis Christoph Kolja Boese, MD, Johannes Oppermann, MD, Jan Siewe, MD, Peer Eysel, MD, Max Joseph Scheyerer, MD, and Philipp Lechler, MD, Cologne, Germany

Spinal cord injury in children is associated with severe morbidity and immense socioeconomic burden. In spinal cord injury without radiologic abnormalities (SCIWORA), magnetic resonance imaging (MRI) can detect intramedullary or extramedullary pathologies or show absence of neuroimaging abnormalities. However, the prognostic and therapeutic consequences of specific MRI patterns are unclear. A comprehensive systematic literature search was performed to examine patient characteristics and imaging patterns of pediatric SCIWORA and to evaluate the prognostic value of a MRI-based classification system. METHODS: MEDLINE, Cochrane Central Register of Controlled Trials, and Google Scholar were searched for studies on SCIWORA in children. Inclusion criteria were (1) traumatic spinal cord injury with acute neurologic deficit, (2) absence of fractures and/or dislocations of the spine, and (3) an immature skeleton or age of less than 18 years. MRI patterns and clinical course were correlated. RESULTS: Forty articles reporting 114 patients were identified. At admission, neurologic deficit assessed by the American Spinal Injury Association impairment scale was A in 28%, B in 17%, C in 31%, and D in 25%. At final follow-up, these were 19%, 6%, 10%, and 16%, respectively. In 43%, no MRI abnormalities (Type I) were detected, and 57% exhibited abnormal scan results (Type II): 6% revealed extraneural (Type IIa), 38% intraneural (Type IIb), and 13% combined abnormalities (Type IIc). At admission and follow-up, American Spinal Injury Association impairment scale differed significantly between the imaging types. CONCLUSION: This systematic review emphasizes the prognostic value of spinal MRI for children with SCIWORA. It highlights the role of the MRI classification system in improving the comparability and interpretability. (J Trauma Acute Care Surg. 2015;78: 874Y882. Copyright * 2015 Wolters Kluwer Health, Inc. All rights reserved.) LEVEL OF EVIDENCE: Systematic review, level IV. KEY WORDS: Spinal cord injury; SCIWORA; child; neuroimaging; MRI; SCIWONA; SCIWORET. BACKGROUND:

S

pinal cord injury (SCI) in children is a challenging condition for the treating surgeon and pediatrician. Despite being rare, with an estimated incidence of 4.6 per million children per year, the associated morbidity, psychological consequences, and the resulting socioeconomic burden can be devastating.1 The immediate radiologic visualization of the spine by plain radiograph or computed tomography (CT) is an essential step in children with SCI.2Y6 In cases of a clinicoradiologic mismatch, that is, patients presenting with SCI without radiologic abnormalities (SCIWORA), the acquisition of early magnetic resonance images of the spine is recommended.3 Magnetic resonance imaging (MRI) allows the further subdivision of SCIWORA into cases with detectable intramedullary or extramedullary pathology and those without neuroimaging abnormalities (SCIWONA),6,7 but the prognostic consequences of specific MRI findings and how they can be used to guide treatment are not yet fully understood. Submitted: August 25, 2014, Revised: December 5, 2014, Accepted: December 8, 2014. From the Department of Orthopaedic and Trauma Surgery (C.K.B., J.O., J.S., P.E., M.J.S.), University Hospital of Cologne, Cologne; Department of Trauma , Hand and Reconstructive Surgery (P.L.), University of Giessen and Marburg, Giessen, Germany. Supplemental digital content is available for this article. Direct URL citations appear in the printed text, and links to the digital files are provided in the HTML text of this article on the journal’s Web site (www.jtrauma.com). Address for reprints: Christoph K. Boese, MD, Department of Orthopaedic and Trauma Surgery, University Hospital of Cologne Kerpener Str. 62 50924 Cologne, Germany; email: [email protected]. DOI: 10.1097/TA.0000000000000579

Furthermore, there is a lack of a consistent classification system for MRI in children with SCIWORA.8 We undertook a comprehensive systematic literature review of SCIWORA in children to establish the clinical characteristics and imaging patterns of the disease and the prognostic value of an MRI classification system.

PATIENTS AND METHODS We conducted a comprehensive computerized search of multiple databases on July 8, 2014, similar to a previously described search strategy and analysis for SCIWORA in adults.8 MEDLINE was searched using PubMed (from 1946 to present), the Internet was searched using Google Scholar (1982Y2014), and the Cochrane Central Register of Controlled Trials was searched using DIMDI (Deutsches Institut fu¨r Medizinische Dokumentation und Information; from 1948 to present). The search strategy for MEDLINE and Cochrane Central Register of Controlled Trials was ‘‘sciwora OR sciworet OR sciwoctet OR sciwona OR spinal cord injury without abnormality OR spinal concussion’’; for Google Scholar it was ‘‘sciwora child,’’ with search parameters that excluded citations and patents. Only results in English or German were included. All search results were recorded in a reference management program (Endnote X7, Thomson Reuters, Carlsbad, CA). The definition of SCIWORA in children was (1) traumatic SCI with acute neurologic deficit; (2) absence of fractures and/or J Trauma Acute Care Surg Volume 78, Number 4

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Figure 1. Flow chart of methodology for identifying publications reporting on SCIWORA in children following the PRISMA guidelines.

dislocations at any spinal level as assessed by plain x-ray, CT or MRI; and (3) an immature skeleton or age less than 18 years. Cases of spinal congenital abnormalities or degenerative changes were not excluded. Only studies providing clinical data of neurologic status at admission and outcome and corresponding MRI findings were included. The database search yielded 1,359 articles (Fig. 1). Duplicates were removed. All titles and abstracts were screened, and publications identified as reviews, editorials, letters or basic science studies were excluded. The full texts of 273 articles were obtained and reviewed by two authors independently (C.K.B., J.O.); 233 were excluded after detailed analysis. The search was expanded to include relevant references cited in these articles; 15 additional potentially eligible publications were identified. Extracted information included demographic data, clinical presentation and neurologic impairment scales at admission and at final follow-up, imaging findings, and therapeutic outcome measures for all individual cases. Information regarding neurologic impairment was allocated a score on the American Spinal Injury Association impairment scale (AIS) by two authors (C.B.K., J.O.) independently; disagreement was resolved through consensus with a third author (P.L.). Improvement was defined as a numeric difference between AIS grade at admission and at final follow-up. Cases were grouped according to MRI patterns

(Table 1), as has been previously described.8 Finally, correlations between individual clinical courses and MRI findings were sought. A subgroup analysis was performed for three age groups: 0 to 3, 4 to 12, and 13 to 17 years.

Statistical Analysis Descriptive statistical analysis was undertaken using Microsoft Excel 2008 for Mac (Microsoft Corporation, Redmond, WA), and exploratory data analysis was performed with GraphPad Prism 5 (GraphPad Software Inc., La Jolla, CA) and SPSS Statistics for Macintosh version 22.0 (IBM Corporation, TABLE 1. Classification of SCIWORA by MRI Type MRI Imaging Type Type I Type IIa Type IIb Type IIc

No detectable abnormalities Extraneural abnormalities Intraneural abnormalities Extraneural and intraneural abnormalities

Adapted from Boese and Lechler8 with permission from Wolters Kluwer. Adaptations are themselves works protected by copyright. So in order to publish this adaptation, authorization must be obtained both from the owner of the copyright in the original work and from the owner of copyright in the translation or adaptation.

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Armonk, NY). Variables were tested for normality using the Kolmogorov-Smirnov test. Ordinal data (i.e., AIS grades) were transformed into numbers (A = 1, B = 2, etc.), and medians with interquartile range (IQR) were given. For independent ordinal non-Gaussian distributed variables, the Kruskal-Wallis test was used. Post hoc analysis was performed by Dunn’s multiple comparison test. A p e 0.05 was considered statistically significant.

RESULTS Forty articles met the inclusion criteria and were retrieved for further analysis (Fig. 1).5,6,9Y46 From these, 114 individual cases with detailed data on all relevant parameters were included in the analysis.

Characteristics of Children With SCIWORA The demographic characteristics, imaging results, and clinical information are presented for each publication in Table 2. Furthermore, the individual clinical and imaging characteristics of all cases are provided (Supplemental Digital Content 1, http://links.lww.com/TA/A535). The sex-specific age distribution is depicted in Figure 2A for 113 cases. The distribution of the highest level of SCI is shown in Figure 2B for 59 cases. Trauma mechanisms are given in Table 2 and depicted for all cases by sex (Fig. 3A) and age (Fig. 3B).

Clinical Course of SCIWORA in Children The clinical courses are presented as AIS grades ranging from A to E. Figure 4 shows the extent to which overall patient outcome depended on the initial neurologic impairment as assessed by the AIS (Supplemental Digital Content 2, http://links.lww.com/TA/A536). The median transformed AIS at admission was 3 (IQR, 2) and at final follow-up was 4 (IQR, 3). The data were nonnormally distributed (p = 0.000). The mean improvement recorded for all patients was 1.1 AIS grades (range, 0Y4). Patients with an initial AIS Grade A had a mean improvement of 0.7 grades (range, 0Y4), the subgroup with initial AIS Grade B improved by an average of 1.8 grades (range, 0Y3), AIS Grade C by 1.3 (range, 0Y2), and AIS Grade D by an average of 0.9 grades (range, 0Y1). At final follow-up, residual neurologic deficits were reported in 87.5%, 63.2%, 45.7%, and 7.1% of the cases with initial AIS Grades A, B, C, and D, respectively. One patient died during follow-up.

MRI Patterns The neuroimaging findings were classified into MRI patterns (Table 1) as has been previously described by Boese and Lechler.8 In 49 patients (43%), no abnormalities were detectable by MRI (Type I), while 65 (57%) had abnormal scan results (Type II). Of these, 7 patients (6%) had extraneural abnormalities alone (Type IIa), while 43 patients (38%) showed isolated intraneural lesions (Type IIb). In 15 patients (13%), combined extraneural and intraneural abnormalities were described (Type IIc) (Table 2; Supplemental Digital Content 1, http://links.lww.com/TA/A535). Four of the extraneural findings were Chiari malformations Type I, and the other 18 were posttraumatic changes. 876

Age-Dependent MRI Patterns The MRI patterns showed an age-dependent distribution. Supplemental Digital Content 3 (http://links.lww.com/TA/A537) provides the age-dependent clinical course with respect to imaging patterns. The distribution of the cases is given in Table 3.

Relation Between MRI Pattern and Clinical Course The initial AIS score and neurologic outcome with regard to MRI findings are shown in Figure 5A to D and Supplemental Digital Content 4 (http://links.lww.com/TA/A538). At admission and at final follow-up, the Kruskal-Wallis test revealed significant differences between the four imaging types (p < 0.0001). Post hoc analysis showed significant differences between Type I and Type IIc and Type IIa/IIb at admission. At final follow-up, post hoc analysis revealed significant differences between Type I/IIb, Type I/IIc, and Type IIa/IIb.

DISCUSSION In traumatic SCI, it is critical to establish an early and reliable diagnosis to guide therapeutic interventions.2 Plain radiographs and CT remain the standard imaging techniques for the visualization of bony injuries.2 In patients presenting with a clinicoradiologic mismatch, MRI has been shown to be a powerful means of identifying soft tissue injuries of the extraneural and intraneural spinal structures.7,8 While it has been suggested that MRI has prognostic value in adult and pediatric acute spinal trauma,3,7,21,22 there is conflicting evidence regarding the importance of distinct MRI patterns in the identification of therapeutic interventions and the reliable prediction of clinical outcome.3,7,21,22 SCIWORA and SCIWORA-like phenomena are of growing scientific interest as underlined by the steady increase in the publications.8 Our comprehensive literature search found detailed clinical and radiologic information on 114 children with SCIWORA. The age distribution was homogenous, and the male-to-female ratio of 2.05:1 concurred with previously reported ratios.1 In the very young, the sex ratio was approximately 1:1, with a male predominance in older individuals, which more closely reflects the ratio of 4.5:1 reported in adults.8 The most common mechanisms of injury were road traffic accidents, followed by sports injuries and fallsVthere was an excess of road traffic accidents in the youngest and sports-related injuries in adolescents. In the 88 cases in which the therapeutic approach was reported, only 3 were managed surgically, and the vast majority (97%) was managed conservatively. Nonetheless, the descriptions of the therapeutic strategies undertaken were often imprecise or incomplete. Current treatment guidelines for patients presenting with SCIWORA are somewhat vague, and individual therapeutic strategies remains common practice.2 While surgery has been recommended in cases with demonstrable spinal cord compression,47 no comparative trials of different treatment options were found. Furthermore, there is a lack of understanding of the optimal means of treating and rehabilitating children with SCIWORA in the subacute phase, despite the critical importance of achieving positive long-term outcomes in pediatric SCI. * 2015 Wolters Kluwer Health, Inc. All rights reserved.

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TABLE 2. Demographic and Clinicoradiologic Characteristics of All Included Studies MRI Type Sex

Trauma Mechanism

II

ID

Author

Year

n

CT

CR

Age

Male

Female

Sport

Fall

RTA

Other

I

a

b

c

Onset

Therapy

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40

Beck Bondurant Boockvar Bosch Buldini Cabarlo Dare Dickerman Dickman Duprez Elgamal Ergun Feldman Felsberg Grabb Grabb Grubenhoff Kalra Kim Koestner Lee Liao Lynch Matsumara Meuli Mortazavi Phillips Piatt Pollack Pollina Rich Riviello Shen Silman Strohm Sullivan Triglylidas Trumble Yalcin Yamaguchi

2000 1993 2001 2002 2006 2005 2002 2006 1991 1998 2008 2003 2008 1995 1994 2000 2008 2006 2008 2001 2006 2005 2004 1990 1991 2011 2013 1995 1988 1999 2006 1990 2007 2008 2003 2008 2010 2000 2011 2002

1 1 13 9 2 1 19 1 2 1 2 1 2 12 7 1 1 1 1 1 1 9 1 1 1 1 2 1 1 1 1 2 1 1 1 2 3 1 3 1

0 0 0 0 1 1 19 1 0 0 2 0 2 12 7 0 1 1 1 1 0 9 0 0 1 1 2 0 0 0 1 2 0 1 0 0 3 1 1 0

1 1 13 0 2 1 19 1 0 1 1 1 1 12 7 1 0 1 1 1 1 0 1 1 1 0 2 1 0 1 1 2 1 0 1 2 3 1 3 1

16.0 2.3 11.5 5.7 1.4 0.4 12.1 14.0 7.0 2.0 9.0 12.0 0.3 9.0 7.4 13.0 7.0 2.5 1.0 1.4 1.2 4.1 0.8 3.0 5.3 1.8 2.0 1.3 9.0 3.0 15.0 2.5 6.0 0.9 14.0 6.0 11.3 2.8 4.2 14.0

0 1 9 6 1 1 16 1 2 1 2 0 0 8 5 1 1 0 0 0 1 6 0 0 0 1 2 0 1 1 1 0 0 1 1 2 2 0 2 0

1 0 4 3 1 0 3 0 0 0 0 1 2 4 2 0 0 1 1 1 0 3 1 1 1 0 0 0 0 0 0 2 1 0 0 0 1 1 1 1

1 0 13 0 0 0 11 1 0 0 0 1 0 1 0 1 1 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 1 0 0 1 1 0 0 0

0 1 0 0 1 0 0 1 0 4 0 1 1 0 0 0 0 1 0 0 0 0 0 2 0 1 0 0 2 0 0 1 1 0 0 0 0 1 0 0

0 0 0 5 1 1 3 0 2 1 2 0 0 9 1 0 0 0 0 0 0 5 0 1 0 1 2 0 0 1 0 0 0 1 0 0 2 1 3 0

0 0 0 2 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 13 0 0 0 17 1 0 0 0 0 0 7 1 1 0 0 0 0 1 3 0 0 1 0 0 0 1 0 0 0 0 0 1 0 0 0 2 0

0 0 0 1 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 1 1 0 0 0

1 0 0 8 1 0 2 0 1 0 2 1 1 3 3 0 1 1 1 0 0 6 1 1 0 0 1 1 0 1 0 1 1 0 0 1 2 1 0 0

0 1 0 0 1 1 0 0 1 1 0 0 1 2 1 0 0 0 0 1 0 0 0 0 0 1 1 0 0 0 0 0 0 1 0 0 0 0 1 1

NA NA NA + + NA NA + NA + j NA + NA NA NA NA + + + + NA NA + NA NA NA NA NA NA j + NA j NA + NA NA NA +

C C C C S NA C+S C NA NA S C S NA C C C C C C C NA C C C C C NA NA C S C C C C NA C C (S) C

Age, mean age at admission in years. Cause, trauma mechanism; RTA, road traffic accident. Applied imaging: CR, conventional roentgen. MRI types: I, no abnormalities; IIa, extraneural abnormalities; IIb, intraneural abnormalities; IIc, intraneural and extraneural abnormalities. Therapy: C, conservative; S, surgical; (S), partly surgical. Onset: negative sign, immediate onset; positive sign, delayed onset. NA, data not available.

The initial AIS grades showed a relatively homogenous distribution of injuries (Grade A, 28%; Grade B, 17%; Grade C, 31%; and Grade D, 25%). At final follow-up, the outcome analysis revealed complete recovery in almost half of the cases (48%). Initial AIS Grade D was associated with excellent outcome (93% fully recovered), while 37% of those with Grade

B and 54% of those with Grade C injuries had good-to-fair outcomes. Only 13% of patients with initial AIS Grade A injury made a complete neurologic recovery, and more than two thirds (69%) made no improvement at all. Our findings underline the importance of the initial neurologic impairment as a prognostic factor for subsequent clinical improvement, closely

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Figure 2. A, Age-dependent distribution by sex in years. B, Distribution by highest level of SCI.

reflecting the clinical course of pediatric and adult patients with spinal cord injuries with radiologic abnormalities and, as recently shown, adults with SCIWORA.8,47 While the use of simplified neurologic grading is convenient and comparable, it might not accurately reflect the magnitude of the neurologic impairment. The mortality rate of all analyzed cases was 1%, rising to 3% in children experiencing complete tetraplegia or paraplegia, less than the mortality of patients experiencing fractureassociated SCI.48 However, some patients with SCIWORA may have died before MRI images could be acquired, and SCIWORA may be underreported in patients with impaired levels of consciousness. To examine the relationship among imaging findings, initial neurologic deficit, and clinical outcome, we applied the recently published MRI classification system (Table 1) for adults to a pediatric population. The current literature reports 49 cases 878

of SCIWORA without neuroimaging abnormalities (Type I), almost equaling the 65 cases with spinal abnormalities on MRI (Types IIa, IIb, and IIc). Despite ongoing improvements in MRI technology, the complete absence of neuroimaging abnormalities remains a relevant clinical phenomenon in children with SCIWORA. Here, the acronym SCIWONA has been proposed to distinguish this subgroup, although it does not further improve our understanding of the condition.5 Importantly, the correlation between the neurologic dysfunction and imaging findings revealed a significantly better prognosis for Type I compared with Type II injuries. In patients with SCIWORA Type II, solitary extraneural (Type IIa) abnormalities were associated with the most favorable outcome, followed by those with combined extraneural and intraneural (Type IIc) lesions. Patients with intraneural (Type IIb) abnormalities had the worst outcomes. Interestingly, in adolescents, SCIWORA Type I occurred in 74% of cases, compared with 20% overall, while * 2015 Wolters Kluwer Health, Inc. All rights reserved.

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Figure 3. A, Trauma mechanism and sex. B, Trauma mechanism and age in years. RTA, road traffic accident; n.a., not applicable.

Figure 4. Initial neurologic impairment and outcome of patients with SCIWORA measured by AIS. Initial: Cumulative distribution of AIS grades at final follow-up (z-axis) of all cases relative to AIS grade at admission (z-axis). Right: Distribution of AIS grade at final follow-up (x-axis) relative to initial AIS (z-axis) with separated depiction for each grade at admission and final follow-up. * 2015 Wolters Kluwer Health, Inc. All rights reserved.

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TABLE 3. Distribution of MRI Types by Age Group MRI Type

Age Group 12

n.a.

n % in group % overall n % in group % overall n % in group % overall n % in group % overall

I

IIa

IIb

IIc

Sum

5 13 4 21 50 18 23 74 20 0 0 0

1 3 1 0 0 0 5 16 4 1 100 1

25 63 22 17 40 15 1 3 1 0 0 0

9 23 8 4 10 4 2 6 2 0 0 0

40 100 35 42 100 37 31 100 27 1 100 1

Percentages of cases per group and overall are given. Sum of each row (n, %) given.

younger children presented more often with intramedullary changes. The distribution of recorded MRI patterns differed considerably from adults with SCIWORA.8 The classification system should be used for future reports to improve the comparability and interpretability of cases of SCIWORA in children. Combining it with other established classification tools for the assessment of intraneural MRI injury pattern might further improve its prognostic value.8,49 While the role of preexisting degenerative changes in adult patients with SCIWORA is a matter of debate,3,4,8 it is unusual in children. In our literature analysis, no such changes were identified. However, congenital spinal stenosis is thought to be a predisposing factor for SCIWORA9,23 and might even pose a vulnerability to recurrent SCIWORA.41 We identified four children with Chiari malformation Type I in the age group of 0 year to 3 years with clinical courses similar to the other cases of the same MRI type.9,23 The best prognostic indicator for outcome following SCIWORA is generally considered to be the initial neurologic status, but recent publications have suggested that spinal MRI is superior.7,8 Our analysis underlines the importance of the prognostic role of MRI.

Figure 5. AYD, Distribution of AIS grade at admission and final follow-up (x-axis) ordered by MRI type. Initial AIS color coded: Grade A, black; B, dark grey; C, middle grey; D, light grey. A, AIS-dependant distribution of cases with MRI Type I. Each bar presents initial AIS Grades A to E relative to the final follow-up AIS grade (x-axis). B, AIS-dependant distribution of cases with MRI Type IIa. Each bar presents initial AIS Grades A to E relative to the final follow-up AIS grade (x-axis). C, AIS-dependant distribution of cases with MRI Type IIb. Each bar presents initial AIS Grades A to E relative to the final follow-up AIS grade (x-axis). D, AIS-dependant distribution of cases with MRI Type IIc. Each bar presents initial AIS Grades A to E relative to the final follow-up AIS grade (x-axis). 880

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The timing of MRI has also been shown to be critical, and serial scans may detect dynamic intramedullary and extramedullary signal changes or previously undetected abnormalities.8 In this context, the concept of delayed-onset SCIWORA is of particular interest: there are reports that clinical symptoms may become evident within minutes of injury but may take as long as 10 days to develop.16,30 We are aware of the limitations of this systematic review. The lack of high-quality studies that provide sufficient detail of MRI findings and the clinical course is a major drawback. No randomized controlled studies were identified, and the majority of reports were retrospective case reports and case series. The strict application of the inclusion criteria led to the exclusion of a substantial proportion of publications. To maximize the number of studies identified in the initial search, a systematic strategy including Google Scholar was undertaken. We also found that the presentation of the neurologic deficits was limited to imprecise clinical descriptions of the impairment in a substantial number of publications, and only few authors used standardized outcome measures. In addition, many articles did not report the precise follow-up periods, and no long-term outcomes of SCIWORA in children are available. Finally, it should be noted that conclusions drawn from any systematic literature search should be interpreted with caution and the presented classification system requires further validation in clinical studies.

CONCLUSION To the best of our knowledge, this is the first systematic and comprehensive review of SCIWORA in children with an emphasis on the correlation between MRI patterns and neurologic outcome. The conclusions are similar to the previously published report on SCIWORA in adults.8 Our study highlights the importance of spinal MRI for children with SCIWORA. A classification system of MRI findings led to excellent comparability with published reports. Statistical analysis revealed a significant association between the extent of initial neurologic impairment, specific MRI patterns, and subsequent outcome. We recommend spinal MRI for all patients experiencing SCIWORA and the application of the classification system for future studies. AUTHORSHIP C.K.B. and P.L. devised the study concept, performed the literature research, conducted the data analysis, and wrote the article. J.O. and M.J.S. conducted the data analysis and critically reviewed the manuscript. J.S. and P.E. critically reviewed the manuscript.

DISCLOSURE The authors declare no conflict of interest.

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