- Email: [email protected]
Influence of Preoperative Magnetic Resonance Imaging on Surgical Decision Making for Patients with Acute Traumatic Cervical Spinal Cord Injury: A Survey Among Experienced Spine Surgeons
Original Article
Influence of Preoperative Magnetic Resonance Imaging on Surgical Decision Making for Patients with Acute Traumatic Cervical Spinal Cord Injury: A Survey Among Experienced Spine Surgeons Lukas Grassner1,3,5,8, Christof Wutte3, Georg Zimmermann6,7, Andreas Grillho¨sl4, Katharina Schmid1, Thomas Weib2, Walter Maier1, Stefan Hauck2, Tobias Hollerith1, Matthias Vogel3, Michael Bierschneider1, Jan Vastmans3, Claudius Thome´8, Oliver Gonschorek2, Martin Strowitzki1
OBJECTIVE: Early decompression after acute spinal cord injury (SCI) is recommended. Acute care is crucial, but optimal management is unclear. The aim of this study was to investigate the role of preoperative magnetic resonance imaging (MRI) in addition to computed tomography (CT) in surgical decision making for acute cervical SCI.
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METHODS: All patients with cervical SCI between 2008 and 2016 who had preoperative CT and MRI (n [ 63) at the Trauma Center Murnau, Germany, were included. We administered a survey to 10 experienced spine surgeons (5 neurosurgeons, 5 trauma surgeons) regarding the surgical management. First, the surgeons were shown clinical information and CT scans. Two months later, the survey was repeated with additional MRI. Corresponding percentages of change and agreement were obtained for each rater and survey item. Finally, results from both parts of the survey were compared with the definitive treatment option (i.e., real-world decision).
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RESULTS: MRI modified surgical timing in a median of 41% of patients (interquartile range 38%e56%). In almost every fifth patient (17%), no surgery would have been indicated with CT alone. The advocated surgical approach was changed in almost half of patients (median 48%, interquartile range 33%e49%). Surgically addressed levels were changed in a median of 57% of patients (interquartile range 56%e60%). MRI led to higher agreement with the
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real-world decision concerning addressed levels (median 35% vs. 73%), timing (median 51% vs. 57%), and approach (median 44% vs. 65%). CONCLUSIONS: Preoperative MRI influenced surgical decision making substantially in our cohort and has become a new standard for patients with cervical SCI in our institution if medically possible.
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INTRODUCTION
S
pinal cord injury (SCI) is a devastating condition for affected individuals, and treatment options remain limited. Currently, early surgical decompression of the spinal canal and restoration of spinal alignment within 24 hours together with the maintenance of adequate mean arterial blood pressure within the acute phase are recommended.1,2 More recent studies advocate an ultra-early decompression within the first 8 hours after cervical SCI.3,4 After cervical trauma without neurologic impairment, computed tomography (CT) alone might be sufficient in most cases to guide clinical decision making.5 However, certain situations, such as in cases involving older patients (>60 years old), nonaccessible clinical examination, preexisting cervical spondylosis, polytrauma, and neurologic deficits, may warrant the additional use of magnetic resonance imaging (MRI).6-8 As there may be a time-dependent effect of surgical decompression after acute SCI,
Key words - Acute care - Cervical spine - Magnetic resonance imaging - Outcome - Spinal cord injury - Trauma
From the 1Department of Neurosurgery, 2Department of Spine Surgery, 3Center for Spinal Cord Injuries, and 4Department of Neuroradiology, BG Trauma Center Murnau, Murnau, Germany; 5Institute for Molecular Regenerative Medicine, 6Spinal Cord Injury and Tissue Regeneration Center Salzburg, and 7Department of Neurology, Christian Doppler Medical Center and Center for Cognitive Neuroscience, Paracelsus Medical University, Salzburg, Austria; and 8Department of Neurosurgery, Medical University Innsbruck, Innsbruck, Austria
Abbreviations and Acronyms CT: Computed tomography MRI: Magnetic resonance imaging SCI: Spinal cord injury
Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.08.009
To whom correspondence should be addressed: Lukas Grassner, M.D., Ph.D. [E-mail: [email protected]]
Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY -: e1-e7, - 2019
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ORIGINAL ARTICLE LUKAS GRASSNER ET AL.
INFLUENCE OF PREOPERATIVE MRI AFTER SCI
surgery is performed promptly in our institution. A CT scan of the cervical spine is part of the routine assessment in almost every hospital. Although osseous injuries can be well characterized by CT, imaging of the injured spinal cord and discoligamentous structures via CT is limited. MRI allows better visualization of these structures.9 However, MRI is time-consuming and often not readily available in the acute setting, especially for intubated and unstable patients.10 MRI is recommended to direct clinical management of patients with acute SCI,11,12 but the evidence is relatively sparse. Hence, some authors advocate surgical management without preoperative MRI to warrant fast decompression if a bony injury is detected.13 The influence on surgical decision making of preoperative MRI in addition to an available CT scan in patients with cervical SCI is not known. Therefore, we performed a survey among experienced spine surgeons (trauma surgeons and neurosurgeons), in which we retrospectively assessed the additional influence of preoperative MRI on surgical timing, surgical approach, and levels to be surgically addressed compared with CT alone. We wanted to assess if preoperative MRI can be considered optional or required.
The survey consisted of the following 4 questions that could be answered by checking 1 of the predefined answers. Furthermore, free commentaries could be included. The questions were as follows: 1. Is a surgical intervention necessary? If yes, when? a. No b. Yes within 8 hours c. Yes within 24 hours d. Yes, throughout the next days but not acutely 2. Would an additional MRI be helpful or do you feel confident to make a treatment decision without it? a. Yes b. No 3. What surgical approach would you perform in this case (with the available clinical and radiologic information)? a. Anterior approach: stand-alone cage b. Anterior approach: cage plus plate and screws c. Anterior approach: corpectomy
MATERIALS AND METHODS Patient Selection Between 2008 and 2016, we retrospectively reviewed all patients with an acute cervical SCI who were managed surgically in the acute phase at the Trauma Center Murnau, Germany, a crossregional level 1 trauma center with a specialized SCI department. To test the influence of preoperative MRI, we included only patients for whom sufficient clinical information plus preoperative CT and MRI scans were available. There were no predefined criteria of required preoperative imaging criteria during the study period. Patients without preoperative MRI were excluded. The responsible Bavarian Ethical Committee agreed to the final study protocol (2018e186). Survey—General Information Patient data including age, sex, comorbidities, anticoagulation, cause of injury, time of injury, time delay until arrival in our institution, neurologic impairment, and other relevant injuries such as traumatic brain injury were presented anonymized to 10 different surgeons. The participants were experienced spine surgeons with a mean experience of 21.3 years (range, 13e34 years). The group was balanced between neurosurgeons and trauma surgeons (5 each), as both specialties perform these surgeries in our institution, most often in interdisciplinary situations. Survey—Part 1 The purpose was to closely simulate the acute situation. Hence, patient information was anonymously presented to all participating surgeons. During the first part of the survey, available CT scans were shown by an experienced neuroradiologist. The surgeons were allowed to ask questions to the presenter and the neuroradiologist about the clinical course and to take a closer look at all planes of the CT scan as often as they wanted. However, the surgeons were not allowed to collaborate in their decision process.
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d. Anterior approach: corpectomy plus plate and screws e. Posterior approach: fusion only f. Posterior approach: decompression only g. Posterior approach: decompression and fusion h. Circumferential approach without decompression i. Circumferential approach with decompression 4. What level of surgery should be performed? Survey—Part 2 With a significant delay of almost 2 months, the selected patient cohort was presented again anonymously to the same surgeons. This time, after the CT scan, the additional MRI scan was shown after the CT scan. The same survey questions were presented again to the surgeons. Statistical Methods At first, for each rater, the results of the CT-only and the CT plus MRI surveys were compared with each other as well as with the real-world decisions (i.e., the treatment option that was chosen for the case) by summarizing the (dis-)agreement descriptively over all patients. Hence, for each rater and each item of the survey, corresponding percentages of change/agreement were obtained. Subsequently, for every item, the median percentage over the 10 raters was calculated, and the results were summarized in tabular forms and corresponding graphic displays. The statistical software package R Version 3.4.114 was used for all analyses. RESULTS After applying inclusion and exclusion criteria, 63 patients with acute cervical SCI were included in the study. Their clinical information was presented, and the survey was undertaken in a
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.08.009
ORIGINAL ARTICLE LUKAS GRASSNER ET AL.
INFLUENCE OF PREOPERATIVE MRI AFTER SCI
Figure 1. Influence on surgical timing. Box plot showing the percentage of changes regarding surgical urgency after showing preoperative magnetic resonance imaging. The overall change and change toward earlier or delayed management are indicated.
2-step fashion as mentioned in Materials and Methods. Most patients sustained discoligamentous injuries (n ¼ 46; 73%). Other patients presented with compression and/or burst fractures (n ¼ 8; 12.7%) and luxation fractures (n ¼ 9; 14.3%). First, we analyzed changes in several aspects of surgical decision making from each surgeon after CT only versus CT plus MRI. Additional radiologic information gained by MRI led to different surgical timing in >40%. In most cases, earlier decompression seemed to be warranted (median 32%). Under some circumstances (e.g., minor cord changes or oral anticoagulation), some surgeons advocated for delayed surgical management (median 11%) (Figure 1). In almost every fifth patient, MRI showed the lesion per se, which led to the decision that surgical management was warranted (median 17%) (Figure 2). After CT alone, no need for surgery would have been seen in these patients. The planned surgical approach was changed in almost half of the cases (median 48%) after additional MRI had been presented (Figure 3). After the second survey, the level or levels that were chosen to be surgically addressed changed in almost 60% of cases. Other levels were identified in one third of patients. In about 25% of cases, MRI allowed the exact localization of the level that should be addressed by surgery. Completely different levels were recognized in a median of 13% (Figure 4). Detailed numerical values are provided in Table 1, and representative images are shown in Figure 5. As a next step, we compared the results of survey 1 and survey 2 with the definitive treatment option that was chosen clinically. When the CT-only group was compared with the CT plus MRI group, we identified a median agreement with the real-world
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Figure 2. Influence on overall surgical decision. Box plot indicating the influence on the surgical decision per se. Without magnetic resonance imaging, no need for surgery would have been seen.
decision (i.e., treatment options that were definitely chosen) in 35% of cases versus 73% regarding the surgically addressed level, in 51% versus 57% of cases regarding the preferred timing of intervention, and in 44% versus 65% of cases concerning the surgical approach (Table 2 and Figure 6).
DISCUSSION Acute care after SCI is probably the most crucial step in the management of these patients. There is accumulating evidence that early surgical intervention might be beneficial for patients with SCI.3,4,15 Owing to this time-dependent effect, the role of preoperative MRI has been debated. This study aimed to investigate the role of preoperative MRI in addition to routinely performed CT in patients with acute cervical SCI. We observed an influential effect of MRI on surgical timing in a relatively high proportion in our study cohort. This seems surprising, as rapid surgical intervention was already being performed in our institution during the study period.3,15 The extent of spinal cord damage apparently influenced the surgical timing, as the surgeons recommended earlier surgical intervention if medullary compression with signal changes was apparent on MRI. Additionally, the potential predictive role of axial and sagittal T2 spinal cord alterations has been demonstrated in the literature.16,17
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INFLUENCE OF PREOPERATIVE MRI AFTER SCI
Figure 4. Influence on addressed surgical levels. Box plot indicating the changes in the addressed level generally as well as regarding the identification of different, exact, and additional anatomic levels that needed to be addressed surgically.
Figure 3. Influence on surgical approach. Box plot indicating the influence of additional preoperative magnetic resonance imaging on the planned surgical approach.
It should be kept in mind that these changes and lesion expansion are dynamic—especially in the acute phase.18-20 Furthermore, diffusion tensor imaging and fractional anisotropy will most likely serve as diagnostic and prognostic surrogate markers in the future.21,22 In almost every fifth case, no clear osseous injury was detectable on CT. In these cases, MRI revealed the traumatic spinal column and spinal cord damage. This was especially true for patients with multiple degenerative imaging findings who presented with clinically incomplete cervical SCI after low-impact trauma. Notably, this is currently the most common form of SCI in Western countries.23 Logically, preoperative MRI is essential for these patients. It is well known that MRI identifies more osseous and soft tissue injuries.24-26 Furthermore, knowledge about the extent of bone marrow edema gained by MRI raises the awareness of potential fracture types and might be beneficial for the evaluation.27 The favored surgical approach differed markedly when the results from CT and MRI examinations together were considered compared with the results of CT only. Additional MRI led to a change in the planned surgical approach in almost 50% of cases. Furthermore, MRI had an impact on the anatomic levels that needed to be addressed surgically. Preoperative MRI allowed the identification of the exact levels, other levels, or completely different levels. Knowledge about the spinal cord
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lesion is essential. It has been recently shown that posterior approaches most often result in better decompression of the spinal cord per se.28 Our findings and results from other studies emphasize the important role of preoperative MRI for surgical planning.29,30 We further compared the results of survey 1 and survey 2 with the real-world decisions. The agreement regarding the levels that had to be addressed was much higher when additional MRI was performed (Table 2 and Figure 6). This reflects the higher sensitivity and specificity of MRI to detect spinal injuries. However, we were surprised about the magnitude of our results (median 35% vs. 73% agreement concerning the addressed anatomic levels and 44% vs. 65% agreement regarding the surgical approach). Additionally, one can see that treatment decisions remain variable even within 1 center and that multiple factors influence surgical decision making. Although we try to perform surgery as early as possible,3,15 the surgical timing did not differ relevantly between the CT-only group and CT plus MRI group when compared with the actual surgical timing (median 51% vs. 57%). For us, this finding illustrates that actual timing is influenced by several external as well as internal factors. As the surgeons were aware of extramural circumstances during the survey, we agree with published results that intramural factors may be an essential contributor to delays.31,32 Notably, performing MRI was not associated with a significant time delay in our previous study owing to the readily known possibility of performing this examination.3 The clinical examination and CT results should allow a focused MRI examination to save time.33
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ORIGINAL ARTICLE LUKAS GRASSNER ET AL.
INFLUENCE OF PREOPERATIVE MRI AFTER SCI
Table 1. Changes in Surgical Decision Making after Additional Magnetic Resonance Imaging Examination Variable
Changes in Patients, Median (IQR)
Timing General
41% (38%e56%)
Earlier
32% (29%e44%)
Later
11% (6%e13%)
Surgical decision per se
17% (6%e25%)
Surgical approach
48% (33%e49%)
Change in addressed level(s) General
57% (56%e60%)
Other level(s)
35% (21%e40%)
Identification of exact level(s)
25% (21%e35%)
Different level(s)
13% (11%e14%)
The influence of magnetic resonance imaging in addition to computed tomography is shown as median percentage in 63 patients among 10 surgeons. IQR, interquartile range.
Figure 5. Representative images showing the benefit of preoperative magnetic resonance imaging (MRI) in addition to computed tomography (CT). (AeD) Panels (A) and (B) as well as panels (C) and (D) show that the lesion and instability could be clearly identified only on MRI. (E and F)
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Several limitations need to be acknowledged when interpreting our results. First, not every patient with cervical SCI has received preoperative MRI (in our center, about 60% have received additional preoperative MRI). It was the surgeon’s decision whether to perform the surgery with or without preoperative MRI. Hence, there is a selection bias within our study population, as we included only patients for whom preoperative CT and MRI examinations were available. This is also reflected by the high number of patients with discoligamentous injuries, where MRI is routinely indicated.9 Additionally, all surgeons work in the same institution with a naturally occurring convergence, which might have influenced the results. Furthermore, the retrospective study design and the selection bias do not allow clear conclusions. However, the presented results of this study changed the acute management in our center, as every patient with cervical SCI will receive combined CT and MRI examination in the future if medically possible. Hence, a similar study with a reduced bias may be repeated in the future. There is accumulating evidence that in several (mostly severely affected) patients, the edematous spinal cord is compressed against the relatively firm spinal dura.34 Hence, a spinal compartment syndrome might develop.35 Additional durotomy with augmentative duroplasty has been proposed for selected patients. Logically, the swollen spinal cord with a diminished
Sagittal CT (E, arrow) and MRI (F) show osseous injury (C7 spinous process fracture) (E) and spinal cord T2 hyperintensity a few levels above C3-4 (F). (G and H) Sagittal CT (G) and MRI (H) show no clear traumatic osseous injury (G), but MRI shows a compressive epidural hematoma (H, arrow).
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INFLUENCE OF PREOPERATIVE MRI AFTER SCI
Table 2. Agreement of Survey 1 (Computed Tomography Only) and Survey 2 (Computed Tomography Plus Magnetic Resonance Imaging) With Final Chosen Treatment Option CT Only, Median (IQR)
CT plus MRI, Median (IQR)
35% (30%e38%)
73% (68%e78%)
Timing
51% (48%e56%)
57% (56%e59%)
Approach
44% (38%e49%)
65% (65%e71%)
Level
CT, computed tomography; IQR, interquartile range; MRI magnetic resonance imaging.
subarachnoid space can be assessed only by MRI. This concept further stresses the important role of MRI examinations in the acute phase after cervical SCI. Optimization of logistics to warrant MRI examination followed by surgical intervention is important. Notably, we have shown that preoperative MRI did
Figure 6. Agreement with real-world decision. Agreement regarding the anatomic level, timing, and surgical approach between the computed tomographyeonly group (survey part 1) and the computed tomography plus magnetic resonance
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not result in a significant delay in our cohort.3 Consequently, patients with acute SCI should be managed only in high-volume interdisciplinary centers where MRI is readily available. CONCLUSIONS The results of this study demonstrate the additional benefit of preoperative MRI in acute cervical SCI. Knowledge gained by MRI directly influenced our surgical decision making as demonstrated by the survey’s results and the comparison with the definitive surgical management (real-world decisions) in our study population. Because of these results, preoperative MRI has become a standard of care in our institution for all patients with cervical SCI. ACKNOWLEDGMENTS We thank Mr. Orpheus Mach for his coordinative support with data management.
imaging group (survey part 2) concerning the treatment option that was chosen for the patient in the clinical setting. CT only, computed tomographyeonly group; CTþMRI, computed tomography plus magnetic resonance imaging group.
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ORIGINAL ARTICLE LUKAS GRASSNER ET AL.
INFLUENCE OF PREOPERATIVE MRI AFTER SCI
patients with acute traumatic spinal cord injury. Glob Spine J. 2017;7(3 Suppl):151S-174S.
REFERENCES 1. Wilson JR, Tetreault LA, Kwon BK, et al. Timing of decompression in patients with acute spinal cord injury: a systematic review. Glob Spine J. 2017; 7(3 Suppl):95S-115S. 2. Walters BC, Hadley MN, Hurlbert RJ, et al. Guidelines for the management of acute cervical spine and spinal cord injuries: 2013 update. Neurosurgery. 2013;60(Suppl 1):82-91. 3. Grassner L, Wutte C, Klein B, et al. Early decompression (< 8 h) after traumatic cervical spinal cord injury improves functional outcome as assessed by spinal cord independence measure after one year. J Neurotrauma. 2016;33:1658-1666. 4. Jug M, Kejzar N, Vesel M, et al. Neurological recovery after traumatic cervical spinal cord injury is superior if surgical decompression and instrumented fusion are performed within 8 hours versus 8 to 24 hours after injury: a single center experience. J Neurotrauma. 2015;32:1385-1392. 5. Schoenfeld AJ, Tobert DG, Le HV, et al. Utility of adding magnetic resonance imaging to computed tomography alone in the evaluation of cervical spine injury: a propensity-matched analysis. Spine (Phila Pa 1976). 2018;43:179-184. 6. Schoenfeld AJ, Bono CM, McGuire KJ, Warholic N, Harris MB. Computed tomography alone versus computed tomography and magnetic resonance imaging in the identification of occult injuries to the cervical spine: a meta-analysis. J Trauma. 2010;68:109-113 [discussion: 113-114]. 7. Oichi T, Oshima Y, Okazaki R, Azuma S. Preexisting severe cervical spinal cord compression is a significant risk factor for severe paralysis development in patients with traumatic cervical spinal cord injury without bone injury: a retrospective cohort study. Eur Spine J. 2016;25:96-102. 8. Lau BPH, Hey HWD, Lau ET, Nee PY, Tan KA, Tan WT. The utility of magnetic resonance imaging in addition to computed tomography scans in the evaluation of cervical spine injuries: a study of obtunded blunt trauma patients. Eur Spine J. 2018;27:1028-1033. 9. Awad BI, Carmody MA, Lubelski D, et al. Adjacent level ligamentous injury associated with traumatic cervical spine fractures: indications for imaging and implications for treatment. World Neurosurg. 2015;84:69-75. 10. Sliker CW, Mirvis SE, Shanmuganathan K. Assessing cervical spine stability in obtunded blunt trauma patients: review of medical literature. Radiology. 2005;234:733-739. 11. Fehlings MG, Martin AR, Tetreault LA, et al. A clinical practice guideline for the management of patients with acute spinal cord injury: recommendations on the role of baseline magnetic resonance imaging in clinical decision making and outcome prediction. Glob Spine J. 2017;7(3 Suppl):221S-230S. 12. Kurpad S, Martin AR, Tetreault LA, et al. Impact of baseline magnetic resonance imaging on neurologic, functional, and safety outcomes in
13. Raslan AM, Nemecek AN. Controversies in the surgical management of spinal cord injuries. Neurol Res Int. 2012;2012:417834. 14. R Development Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation of Statistica Computing; 2017. 15. Wutte C, Klein B, Becker J, et al. Earlier decompression (<8 hours) results in better neurological and functional outcome after traumatic thoracolumbar spinal cord injury. J Neurotrauma. 2019; 36:2020-2027. 16. Mabray MC, Talbott JF, Whetstone WD, et al. Multidimensional analysis of magnetic resonance imaging predicts early impairment in thoracic and thoracolumbar spinal cord injury. J Neurotrauma. 2016;33:954-962. 17. Talbott JF, Whetstone WD, Readdy WJ, et al. The brain and spinal injury center score: a novel, simple, and reproducible method for assessing the severity of acute cervical spinal cord injury with axial T2-weighted MRI findings. J Neurosurg Spine. 2015;23:495-504.
27. Brinckman MA, Chau C, Ross JS. Marrow edema variability in acute spine fractures. Spine J. 2015;15: 454-460. 28. Aarabi B, Olexa J, Chryssikos T, et al. Extent of spinal cord decompression in motor complete (American Spinal Injury Association Impairment Scale grades A and B) traumatic spinal cord injury patients: post-operative magnetic resonance imaging analysis of standard operative approaches. J Neurotrauma. 2019;36:862-876. 29. Mascarenhas D, Dreizin D, Bodanapally UK, Stein DM. Parsing the utility of CT and MRI in the subaxial cervical spine injury classification (SLIC) system: is CT SLIC enough? AJR Am J Roentgenol. 2016;206:1292-1297. 30. Nouri A, Martin AR, Nater A, et al. Influence of magnetic resonance imaging features on surgical decision-making in degenerative cervical myelopathy: results from a global survey of AOSpine international members. World Neurosurg. 2017;105: 864-874. 31. Samuel AM, Bohl DD, Basques BA, et al. Analysis of delays to surgery for cervical spinal cord injuries. Spine (Phila Pa 1976). 2015;40:992-1000.
18. Rutges J, Kwon BK, Heran M, Ailon T, Street JT, Dvorak MF. A prospective serial MRI study following acute traumatic cervical spinal cord injury. Eur Spine J. 2017;26:2324-2332.
32. Furlan JC, Tung K, Fehlings MG. Process benchmarking appraisal of surgical decompression of spinal cord following traumatic cervical spinal cord injury: opportunities to reduce delays in surgical management. J Neurotrauma. 2013;30:487-491.
19. Aarabi B, Simard JM, Kufera JA, et al. Intramedullary lesion expansion on magnetic resonance imaging in patients with motor complete cervical spinal cord injury. J Neurosurg Spine. 2012; 17:243-250.
33. Khurana B, Karim SM, Zampini JM, et al. Is focused magnetic resonance imaging adequate for treatment decision making in acute traumatic thoracic and lumbar spine fractures seen on whole spine computed tomography? Spine J. 2019;19:403-410.
20. Le E, Aarabi B, Hersh DS, et al. Predictors of intramedullary lesion expansion rate on MR images of patients with subaxial spinal cord injury. J Neurosurg Spine. 2015;22:611-621.
34. Grassner L, Grillhosl A, Griessenauer CJ, et al. Spinal meninges and their role in spinal cord injury: a neuroanatomical review. J Neurotrauma. 2018;35:403-410.
21. Vedantam A, Eckardt G, Wang MC, Schmit BD, Kurpad SN. Clinical correlates of high cervical fractional anisotropy in acute cervical spinal cord injury. World Neurosurg. 2015;83:824-828.
35. Grassner L, Winkler PA, Strowitzki M, Buhren V, Maier D, Bierschneider M. Increased intrathecal pressure after traumatic spinal cord injury: an illustrative case presentation and a review of the literature. Eur Spine J. 2017;26:20-25.
22. Vedantam A, Jirjis MB, Schmit BD, Wang MC, Ulmer JL, Kurpad SN. Diffusion tensor imaging of the spinal cord: insights from animal and human studies. Neurosurgery. 2014;74:1-8 [discussion: 8; quiz 8]. 23. Spinal cord injury (SCI) 2016 facts and figures at a Glance. J Spinal Cord Med. 2016;39:493-494. 24. Koyanagi I, Iwasaki Y, Hida K, Akino M, Imamura H, Abe H. Acute cervical cord injury without fracture or dislocation of the spinal column. J Neurosurg. 2000;93(1 Suppl):15-20. 25. Morais DF, de Melo Neto JS, Meguins LC, Mussi SE, Filho JR, Tognola WA. Clinical applicability of magnetic resonance imaging in acute spinal cord trauma. Eur Spine J. 2014;23:1457-1463. 26. Martinez-Perez R, Munarriz PM, Paredes I, Cotrina J, Lagares A. Cervical spinal cord injury without computed tomography evidence of trauma in adults: magnetic resonance imaging prognostic factors. World Neurosurg. 2017;99:192-199.
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Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Portions of this work were presented at the Annual Spine Conference of the German Society for Neurosurgery on September 14, 2018, in Hamburg, Germany. Received 14 July 2019; accepted 1 August 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.08.009 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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Influence of Preoperative Magnetic Resonance Imaging on Surgical Decision Making for Patients with Acute Traumatic Cervical Spinal Cord Injury: A Survey Among Experienced Spine Surgeons Lukas Grassner1,3,5,8, Christof Wutte3, Georg Zimmermann6,7, Andreas Grillho¨sl4, Katharina Schmid1, Thomas Weib2, Walter Maier1, Stefan Hauck2, Tobias Hollerith1, Matthias Vogel3, Michael Bierschneider1, Jan Vastmans3, Claudius Thome´8, Oliver Gonschorek2, Martin Strowitzki1
OBJECTIVE: Early decompression after acute spinal cord injury (SCI) is recommended. Acute care is crucial, but optimal management is unclear. The aim of this study was to investigate the role of preoperative magnetic resonance imaging (MRI) in addition to computed tomography (CT) in surgical decision making for acute cervical SCI.
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METHODS: All patients with cervical SCI between 2008 and 2016 who had preoperative CT and MRI (n [ 63) at the Trauma Center Murnau, Germany, were included. We administered a survey to 10 experienced spine surgeons (5 neurosurgeons, 5 trauma surgeons) regarding the surgical management. First, the surgeons were shown clinical information and CT scans. Two months later, the survey was repeated with additional MRI. Corresponding percentages of change and agreement were obtained for each rater and survey item. Finally, results from both parts of the survey were compared with the definitive treatment option (i.e., real-world decision).
-
RESULTS: MRI modified surgical timing in a median of 41% of patients (interquartile range 38%e56%). In almost every fifth patient (17%), no surgery would have been indicated with CT alone. The advocated surgical approach was changed in almost half of patients (median 48%, interquartile range 33%e49%). Surgically addressed levels were changed in a median of 57% of patients (interquartile range 56%e60%). MRI led to higher agreement with the
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real-world decision concerning addressed levels (median 35% vs. 73%), timing (median 51% vs. 57%), and approach (median 44% vs. 65%). CONCLUSIONS: Preoperative MRI influenced surgical decision making substantially in our cohort and has become a new standard for patients with cervical SCI in our institution if medically possible.
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INTRODUCTION
S
pinal cord injury (SCI) is a devastating condition for affected individuals, and treatment options remain limited. Currently, early surgical decompression of the spinal canal and restoration of spinal alignment within 24 hours together with the maintenance of adequate mean arterial blood pressure within the acute phase are recommended.1,2 More recent studies advocate an ultra-early decompression within the first 8 hours after cervical SCI.3,4 After cervical trauma without neurologic impairment, computed tomography (CT) alone might be sufficient in most cases to guide clinical decision making.5 However, certain situations, such as in cases involving older patients (>60 years old), nonaccessible clinical examination, preexisting cervical spondylosis, polytrauma, and neurologic deficits, may warrant the additional use of magnetic resonance imaging (MRI).6-8 As there may be a time-dependent effect of surgical decompression after acute SCI,
Key words - Acute care - Cervical spine - Magnetic resonance imaging - Outcome - Spinal cord injury - Trauma
From the 1Department of Neurosurgery, 2Department of Spine Surgery, 3Center for Spinal Cord Injuries, and 4Department of Neuroradiology, BG Trauma Center Murnau, Murnau, Germany; 5Institute for Molecular Regenerative Medicine, 6Spinal Cord Injury and Tissue Regeneration Center Salzburg, and 7Department of Neurology, Christian Doppler Medical Center and Center for Cognitive Neuroscience, Paracelsus Medical University, Salzburg, Austria; and 8Department of Neurosurgery, Medical University Innsbruck, Innsbruck, Austria
Abbreviations and Acronyms CT: Computed tomography MRI: Magnetic resonance imaging SCI: Spinal cord injury
Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.08.009
To whom correspondence should be addressed: Lukas Grassner, M.D., Ph.D. [E-mail: [email protected]]
Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY -: e1-e7, - 2019
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ORIGINAL ARTICLE LUKAS GRASSNER ET AL.
INFLUENCE OF PREOPERATIVE MRI AFTER SCI
surgery is performed promptly in our institution. A CT scan of the cervical spine is part of the routine assessment in almost every hospital. Although osseous injuries can be well characterized by CT, imaging of the injured spinal cord and discoligamentous structures via CT is limited. MRI allows better visualization of these structures.9 However, MRI is time-consuming and often not readily available in the acute setting, especially for intubated and unstable patients.10 MRI is recommended to direct clinical management of patients with acute SCI,11,12 but the evidence is relatively sparse. Hence, some authors advocate surgical management without preoperative MRI to warrant fast decompression if a bony injury is detected.13 The influence on surgical decision making of preoperative MRI in addition to an available CT scan in patients with cervical SCI is not known. Therefore, we performed a survey among experienced spine surgeons (trauma surgeons and neurosurgeons), in which we retrospectively assessed the additional influence of preoperative MRI on surgical timing, surgical approach, and levels to be surgically addressed compared with CT alone. We wanted to assess if preoperative MRI can be considered optional or required.
The survey consisted of the following 4 questions that could be answered by checking 1 of the predefined answers. Furthermore, free commentaries could be included. The questions were as follows: 1. Is a surgical intervention necessary? If yes, when? a. No b. Yes within 8 hours c. Yes within 24 hours d. Yes, throughout the next days but not acutely 2. Would an additional MRI be helpful or do you feel confident to make a treatment decision without it? a. Yes b. No 3. What surgical approach would you perform in this case (with the available clinical and radiologic information)? a. Anterior approach: stand-alone cage b. Anterior approach: cage plus plate and screws c. Anterior approach: corpectomy
MATERIALS AND METHODS Patient Selection Between 2008 and 2016, we retrospectively reviewed all patients with an acute cervical SCI who were managed surgically in the acute phase at the Trauma Center Murnau, Germany, a crossregional level 1 trauma center with a specialized SCI department. To test the influence of preoperative MRI, we included only patients for whom sufficient clinical information plus preoperative CT and MRI scans were available. There were no predefined criteria of required preoperative imaging criteria during the study period. Patients without preoperative MRI were excluded. The responsible Bavarian Ethical Committee agreed to the final study protocol (2018e186). Survey—General Information Patient data including age, sex, comorbidities, anticoagulation, cause of injury, time of injury, time delay until arrival in our institution, neurologic impairment, and other relevant injuries such as traumatic brain injury were presented anonymized to 10 different surgeons. The participants were experienced spine surgeons with a mean experience of 21.3 years (range, 13e34 years). The group was balanced between neurosurgeons and trauma surgeons (5 each), as both specialties perform these surgeries in our institution, most often in interdisciplinary situations. Survey—Part 1 The purpose was to closely simulate the acute situation. Hence, patient information was anonymously presented to all participating surgeons. During the first part of the survey, available CT scans were shown by an experienced neuroradiologist. The surgeons were allowed to ask questions to the presenter and the neuroradiologist about the clinical course and to take a closer look at all planes of the CT scan as often as they wanted. However, the surgeons were not allowed to collaborate in their decision process.
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d. Anterior approach: corpectomy plus plate and screws e. Posterior approach: fusion only f. Posterior approach: decompression only g. Posterior approach: decompression and fusion h. Circumferential approach without decompression i. Circumferential approach with decompression 4. What level of surgery should be performed? Survey—Part 2 With a significant delay of almost 2 months, the selected patient cohort was presented again anonymously to the same surgeons. This time, after the CT scan, the additional MRI scan was shown after the CT scan. The same survey questions were presented again to the surgeons. Statistical Methods At first, for each rater, the results of the CT-only and the CT plus MRI surveys were compared with each other as well as with the real-world decisions (i.e., the treatment option that was chosen for the case) by summarizing the (dis-)agreement descriptively over all patients. Hence, for each rater and each item of the survey, corresponding percentages of change/agreement were obtained. Subsequently, for every item, the median percentage over the 10 raters was calculated, and the results were summarized in tabular forms and corresponding graphic displays. The statistical software package R Version 3.4.114 was used for all analyses. RESULTS After applying inclusion and exclusion criteria, 63 patients with acute cervical SCI were included in the study. Their clinical information was presented, and the survey was undertaken in a
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.08.009
ORIGINAL ARTICLE LUKAS GRASSNER ET AL.
INFLUENCE OF PREOPERATIVE MRI AFTER SCI
Figure 1. Influence on surgical timing. Box plot showing the percentage of changes regarding surgical urgency after showing preoperative magnetic resonance imaging. The overall change and change toward earlier or delayed management are indicated.
2-step fashion as mentioned in Materials and Methods. Most patients sustained discoligamentous injuries (n ¼ 46; 73%). Other patients presented with compression and/or burst fractures (n ¼ 8; 12.7%) and luxation fractures (n ¼ 9; 14.3%). First, we analyzed changes in several aspects of surgical decision making from each surgeon after CT only versus CT plus MRI. Additional radiologic information gained by MRI led to different surgical timing in >40%. In most cases, earlier decompression seemed to be warranted (median 32%). Under some circumstances (e.g., minor cord changes or oral anticoagulation), some surgeons advocated for delayed surgical management (median 11%) (Figure 1). In almost every fifth patient, MRI showed the lesion per se, which led to the decision that surgical management was warranted (median 17%) (Figure 2). After CT alone, no need for surgery would have been seen in these patients. The planned surgical approach was changed in almost half of the cases (median 48%) after additional MRI had been presented (Figure 3). After the second survey, the level or levels that were chosen to be surgically addressed changed in almost 60% of cases. Other levels were identified in one third of patients. In about 25% of cases, MRI allowed the exact localization of the level that should be addressed by surgery. Completely different levels were recognized in a median of 13% (Figure 4). Detailed numerical values are provided in Table 1, and representative images are shown in Figure 5. As a next step, we compared the results of survey 1 and survey 2 with the definitive treatment option that was chosen clinically. When the CT-only group was compared with the CT plus MRI group, we identified a median agreement with the real-world
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Figure 2. Influence on overall surgical decision. Box plot indicating the influence on the surgical decision per se. Without magnetic resonance imaging, no need for surgery would have been seen.
decision (i.e., treatment options that were definitely chosen) in 35% of cases versus 73% regarding the surgically addressed level, in 51% versus 57% of cases regarding the preferred timing of intervention, and in 44% versus 65% of cases concerning the surgical approach (Table 2 and Figure 6).
DISCUSSION Acute care after SCI is probably the most crucial step in the management of these patients. There is accumulating evidence that early surgical intervention might be beneficial for patients with SCI.3,4,15 Owing to this time-dependent effect, the role of preoperative MRI has been debated. This study aimed to investigate the role of preoperative MRI in addition to routinely performed CT in patients with acute cervical SCI. We observed an influential effect of MRI on surgical timing in a relatively high proportion in our study cohort. This seems surprising, as rapid surgical intervention was already being performed in our institution during the study period.3,15 The extent of spinal cord damage apparently influenced the surgical timing, as the surgeons recommended earlier surgical intervention if medullary compression with signal changes was apparent on MRI. Additionally, the potential predictive role of axial and sagittal T2 spinal cord alterations has been demonstrated in the literature.16,17
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ORIGINAL ARTICLE LUKAS GRASSNER ET AL.
INFLUENCE OF PREOPERATIVE MRI AFTER SCI
Figure 4. Influence on addressed surgical levels. Box plot indicating the changes in the addressed level generally as well as regarding the identification of different, exact, and additional anatomic levels that needed to be addressed surgically.
Figure 3. Influence on surgical approach. Box plot indicating the influence of additional preoperative magnetic resonance imaging on the planned surgical approach.
It should be kept in mind that these changes and lesion expansion are dynamic—especially in the acute phase.18-20 Furthermore, diffusion tensor imaging and fractional anisotropy will most likely serve as diagnostic and prognostic surrogate markers in the future.21,22 In almost every fifth case, no clear osseous injury was detectable on CT. In these cases, MRI revealed the traumatic spinal column and spinal cord damage. This was especially true for patients with multiple degenerative imaging findings who presented with clinically incomplete cervical SCI after low-impact trauma. Notably, this is currently the most common form of SCI in Western countries.23 Logically, preoperative MRI is essential for these patients. It is well known that MRI identifies more osseous and soft tissue injuries.24-26 Furthermore, knowledge about the extent of bone marrow edema gained by MRI raises the awareness of potential fracture types and might be beneficial for the evaluation.27 The favored surgical approach differed markedly when the results from CT and MRI examinations together were considered compared with the results of CT only. Additional MRI led to a change in the planned surgical approach in almost 50% of cases. Furthermore, MRI had an impact on the anatomic levels that needed to be addressed surgically. Preoperative MRI allowed the identification of the exact levels, other levels, or completely different levels. Knowledge about the spinal cord
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lesion is essential. It has been recently shown that posterior approaches most often result in better decompression of the spinal cord per se.28 Our findings and results from other studies emphasize the important role of preoperative MRI for surgical planning.29,30 We further compared the results of survey 1 and survey 2 with the real-world decisions. The agreement regarding the levels that had to be addressed was much higher when additional MRI was performed (Table 2 and Figure 6). This reflects the higher sensitivity and specificity of MRI to detect spinal injuries. However, we were surprised about the magnitude of our results (median 35% vs. 73% agreement concerning the addressed anatomic levels and 44% vs. 65% agreement regarding the surgical approach). Additionally, one can see that treatment decisions remain variable even within 1 center and that multiple factors influence surgical decision making. Although we try to perform surgery as early as possible,3,15 the surgical timing did not differ relevantly between the CT-only group and CT plus MRI group when compared with the actual surgical timing (median 51% vs. 57%). For us, this finding illustrates that actual timing is influenced by several external as well as internal factors. As the surgeons were aware of extramural circumstances during the survey, we agree with published results that intramural factors may be an essential contributor to delays.31,32 Notably, performing MRI was not associated with a significant time delay in our previous study owing to the readily known possibility of performing this examination.3 The clinical examination and CT results should allow a focused MRI examination to save time.33
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ORIGINAL ARTICLE LUKAS GRASSNER ET AL.
INFLUENCE OF PREOPERATIVE MRI AFTER SCI
Table 1. Changes in Surgical Decision Making after Additional Magnetic Resonance Imaging Examination Variable
Changes in Patients, Median (IQR)
Timing General
41% (38%e56%)
Earlier
32% (29%e44%)
Later
11% (6%e13%)
Surgical decision per se
17% (6%e25%)
Surgical approach
48% (33%e49%)
Change in addressed level(s) General
57% (56%e60%)
Other level(s)
35% (21%e40%)
Identification of exact level(s)
25% (21%e35%)
Different level(s)
13% (11%e14%)
The influence of magnetic resonance imaging in addition to computed tomography is shown as median percentage in 63 patients among 10 surgeons. IQR, interquartile range.
Figure 5. Representative images showing the benefit of preoperative magnetic resonance imaging (MRI) in addition to computed tomography (CT). (AeD) Panels (A) and (B) as well as panels (C) and (D) show that the lesion and instability could be clearly identified only on MRI. (E and F)
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Several limitations need to be acknowledged when interpreting our results. First, not every patient with cervical SCI has received preoperative MRI (in our center, about 60% have received additional preoperative MRI). It was the surgeon’s decision whether to perform the surgery with or without preoperative MRI. Hence, there is a selection bias within our study population, as we included only patients for whom preoperative CT and MRI examinations were available. This is also reflected by the high number of patients with discoligamentous injuries, where MRI is routinely indicated.9 Additionally, all surgeons work in the same institution with a naturally occurring convergence, which might have influenced the results. Furthermore, the retrospective study design and the selection bias do not allow clear conclusions. However, the presented results of this study changed the acute management in our center, as every patient with cervical SCI will receive combined CT and MRI examination in the future if medically possible. Hence, a similar study with a reduced bias may be repeated in the future. There is accumulating evidence that in several (mostly severely affected) patients, the edematous spinal cord is compressed against the relatively firm spinal dura.34 Hence, a spinal compartment syndrome might develop.35 Additional durotomy with augmentative duroplasty has been proposed for selected patients. Logically, the swollen spinal cord with a diminished
Sagittal CT (E, arrow) and MRI (F) show osseous injury (C7 spinous process fracture) (E) and spinal cord T2 hyperintensity a few levels above C3-4 (F). (G and H) Sagittal CT (G) and MRI (H) show no clear traumatic osseous injury (G), but MRI shows a compressive epidural hematoma (H, arrow).
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ORIGINAL ARTICLE LUKAS GRASSNER ET AL.
INFLUENCE OF PREOPERATIVE MRI AFTER SCI
Table 2. Agreement of Survey 1 (Computed Tomography Only) and Survey 2 (Computed Tomography Plus Magnetic Resonance Imaging) With Final Chosen Treatment Option CT Only, Median (IQR)
CT plus MRI, Median (IQR)
35% (30%e38%)
73% (68%e78%)
Timing
51% (48%e56%)
57% (56%e59%)
Approach
44% (38%e49%)
65% (65%e71%)
Level
CT, computed tomography; IQR, interquartile range; MRI magnetic resonance imaging.
subarachnoid space can be assessed only by MRI. This concept further stresses the important role of MRI examinations in the acute phase after cervical SCI. Optimization of logistics to warrant MRI examination followed by surgical intervention is important. Notably, we have shown that preoperative MRI did
Figure 6. Agreement with real-world decision. Agreement regarding the anatomic level, timing, and surgical approach between the computed tomographyeonly group (survey part 1) and the computed tomography plus magnetic resonance
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not result in a significant delay in our cohort.3 Consequently, patients with acute SCI should be managed only in high-volume interdisciplinary centers where MRI is readily available. CONCLUSIONS The results of this study demonstrate the additional benefit of preoperative MRI in acute cervical SCI. Knowledge gained by MRI directly influenced our surgical decision making as demonstrated by the survey’s results and the comparison with the definitive surgical management (real-world decisions) in our study population. Because of these results, preoperative MRI has become a standard of care in our institution for all patients with cervical SCI. ACKNOWLEDGMENTS We thank Mr. Orpheus Mach for his coordinative support with data management.
imaging group (survey part 2) concerning the treatment option that was chosen for the patient in the clinical setting. CT only, computed tomographyeonly group; CTþMRI, computed tomography plus magnetic resonance imaging group.
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ORIGINAL ARTICLE LUKAS GRASSNER ET AL.
INFLUENCE OF PREOPERATIVE MRI AFTER SCI
patients with acute traumatic spinal cord injury. Glob Spine J. 2017;7(3 Suppl):151S-174S.
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22. Vedantam A, Jirjis MB, Schmit BD, Wang MC, Ulmer JL, Kurpad SN. Diffusion tensor imaging of the spinal cord: insights from animal and human studies. Neurosurgery. 2014;74:1-8 [discussion: 8; quiz 8]. 23. Spinal cord injury (SCI) 2016 facts and figures at a Glance. J Spinal Cord Med. 2016;39:493-494. 24. Koyanagi I, Iwasaki Y, Hida K, Akino M, Imamura H, Abe H. Acute cervical cord injury without fracture or dislocation of the spinal column. J Neurosurg. 2000;93(1 Suppl):15-20. 25. Morais DF, de Melo Neto JS, Meguins LC, Mussi SE, Filho JR, Tognola WA. Clinical applicability of magnetic resonance imaging in acute spinal cord trauma. Eur Spine J. 2014;23:1457-1463. 26. Martinez-Perez R, Munarriz PM, Paredes I, Cotrina J, Lagares A. Cervical spinal cord injury without computed tomography evidence of trauma in adults: magnetic resonance imaging prognostic factors. World Neurosurg. 2017;99:192-199.
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Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Portions of this work were presented at the Annual Spine Conference of the German Society for Neurosurgery on September 14, 2018, in Hamburg, Germany. Received 14 July 2019; accepted 1 August 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.08.009 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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