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Time is spine: a review of translational advances in spinal cord injury

JNSPG 75th Anniversary Invited Review Article

Jetan H. Badhiwala, Christopher S. Ahuja and Michael G. Fehlings

Acute traumatic spinal cord injury (SCI) is a devastating event with far-reaching physical, emotional, and economic consequences for patients, families, and society at large. Timely delivery of specialized care has reduced mortality; however, long-term neurological recovery continues to be limited. In recent years, a number of exciting neuroprotective and regenerative strategies have emerged and have come under active investigation in clinical trials, and several more are coming down the translational pipeline. Among ongoing trials are RISCIS (riluzole), INSPIRE (Neuro-Spinal Scaffold), MASC (minocycline), and SPRING (VX-210). Microstructural MRI techniques have improved our ability to image the injured spinal cord at high resolution. This innovation, combined with serum and cerebrospinal fluid (CSF) analysis, holds the promise of providing a quantitative biomarker readout of spinal cord neural tissue injury, which may improve prognostication and facilitate stratification of patients for enrollment into clinical trials. Given evidence of the effectiveness of early surgical decompression and growing recognition of the concept that “time is spine,” infrastructural changes at a systems level are being implemented in many regions around the world to provide a streamlined process for transfer of patients with acute SCI to a specialized unit. With the continued aging of the population, central cord syndrome is soon expected to become the most common form of acute traumatic SCI; characterization of the pathophysiology, natural history, and optimal treatment of these injuries is hence a key public health priority. Collaborative international efforts have led to the development of clinical practice guidelines for traumatic SCI based on robust evaluation of current evidence. The current article provides an in-depth review of progress in SCI, covering the above areas.

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Christopher Paul O'Boynick, Mark F. Kurd, Bruce V. Darden II, Alexander R. Vaccaro and Michael G. Fehlings

The understanding of the optimal surgical timing for stabilization in thoracolumbar fractures is severely limited. Thoracolumbar spine fractures can be devastating injuries and are often associated with significant morbidity and mortality. The role of early surgical stabilization (within 48–72 hours of injury) as a vehicle to improve outcomes in these patients has generated significant interest. Goals of early stabilization include improved neurological recovery, faster pulmonary recovery, improved pain control, and decreased health care costs. Opponents cite the potential for increased bleeding, hypotension, and the risk of further cord injury as a few factors that weigh against early stabilization. The concept of spinal cord injury and its relationship to surgical timing remains in question. However, when neurological outcomes are eliminated from the equation, certain measures have shown positive influences from prompt surgical fixation.

Early fixation of thoracolumbar spine fractures can significantly decrease the duration of hospital stay and the number of days in the intensive care unit. Additionally, prompt stabilization can reduce rates of pulmonary complications. This includes decreased rates of pneumonia and fewer days on ventilator support. Cost analysis revealed as much as $80,000 in savings per patient with early stabilization. All of these benefits come without an increase in morbidity or evidence of increased mortality. In addition, there is no evidence that early stabilization has any ill effect on the injured or uninjured spinal cord. Based on the existing data, early fixation of thoracolumbar fractures has been linked with positive outcomes without clear evidence of negative impacts on the patient's neurological status, associated morbidities, or mortality. These procedures can be viewed as “damage control” and may consist of simple posterior instrumentation or open reductions with internal fixation as indicated. Based on the current literature it is advisable to proceed with early surgical stabilization of thoracolumbar fractures in a well-resuscitated patient, unless extenuating medical conditions would prevent it.

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Michael G. Fehlings and Randolph J. Gray

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Editorial

Surgical complications in adult spondylolisthesis

Michael G. Fehlings and Doron Rabin

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George M. Ghobrial, Christopher M. Maulucci, Mitchell Maltenfort, Richard T. Dalyai, Alexander R. Vaccaro, Michael G. Fehlings, John Street, Paul M. Arnold and James S. Harrop

Object

Thoracolumbar spine injuries are commonly encountered in patients with trauma, accounting for almost 90% of all spinal fractures. Thoracolumbar burst fractures comprise a high percentage of these traumatic fractures (45%), and approximately half of the patients with this injury pattern are neurologically intact. However, a debate over complication rates associated with operative versus nonoperative management of various thoracolumbar fracture morphologies is ongoing, particularly concerning those patients presenting without a neurological deficit.

Methods

A MEDLINE search for pertinent literature published between 1966 and December 2013 was conducted by 2 authors (G.G. and R.D.), who used 2 broad search terms to maximize the initial pool of manuscripts for screening. These terms were “operative lumbar spine adverse events” and “nonoperative lumbar spine adverse events.”

Results

In an advanced MEDLINE search of the term “operative lumbar spine adverse events” on January 8, 2014, 1459 results were obtained. In a search of “nonoperative lumbar spine adverse events,” 150 results were obtained. After a review of all abstracts for relevance to traumatic thoracolumbar spinal injuries, 62 abstracts were reviewed for the “operative” group and 21 abstracts were reviewed for the “nonoperative” group. A total of 14 manuscripts that met inclusion criteria for the operative group and 5 manuscripts that met criteria for the nonoperative group were included.

There were a total of 919 and 436 patients in the operative and nonoperative treatment groups, respectively. There were no statistically significant differences between the groups with respect to age, sex, and length of stay. The mean ages were 43.17 years in the operative and 34.68 years in the nonoperative groups. The majority of patients in both groups were Frankel Grade E (342 and 319 in operative and nonoperative groups, respectively). Among the studies that reported the data, the mean length of stay was 14 days in the operative group and 20.75 in the nonoperative group.

The incidence of all complications in the operative and nonoperative groups was 300 (32.6%) and 21 (4.8%), respectively (p = 0.1065). There was no significant difference between the 2 groups with respect to the incidence of pulmonary, thromboembolic, cardiac, and gastrointestinal complications. However, the incidence of infections (pneumonia, urinary tract infection, wound infection, and sepsis) was significantly higher in the operative group (p = 0.000875). The incidence of instrumentation failure and need for revision surgery was 4.35% (40 of 919), a significant morbidity, and an event unique to the operative category (p = 0.00396).

Conclusions

Due to the limited number of high-quality studies, conclusions related to complication rates of operative and nonoperative management of thoracolumbar traumatic injuries cannot be definitively made. Further prospective, randomized studies of operative versus nonoperative management of thoracolumbar and lumbar spine trauma, with standardized definitions of complications and matched patient cohorts, will aid in properly defining the risk-benefit ratio of surgery for thoracolumbar spine fractures.

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Jetan H. Badhiwala, Farshad Nassiri, Christopher D. Witiw, Alireza Mansouri, Saleh A. Almenawer, Leodante da Costa, Michael G. Fehlings and Jefferson R. Wilson

OBJECTIVE

Intraoperative neurophysiological monitoring (IONM) is a useful adjunct in spine surgery, with proven benefit in scoliosis-correction surgery. However, its utility for anterior cervical discectomy and fusion (ACDF) is unclear, as there are few head-to-head comparisons of ACDF outcomes with and without the use of IONM. The authors sought to evaluate the impact of IONM on the safety and cost of ACDF.

METHODS

This was a retrospective analysis of data from the National (Nationwide) Inpatient Sample of the Healthcare Cost and Utilization Project from 2009 to 2013. Patients with a primary procedure code for ACDF were identified, and diagnosis codes were searched to identify cases with postoperative neurological complications. The authors performed univariate and multivariate logistic regression for postoperative neurological complications with use of IONM as the independent variable; additional covariates included age, sex, surgical indication, multilevel fusion, Charlson Comorbidity Index (CCI) score, and admission type. They also conducted propensity score matching in a 1:1 ratio (nearest neighbor) with the use of IONM as the treatment indicator and the aforementioned variables as covariates. In the propensity score–matched cohort, they compared neurological complications, length of stay (LOS), and hospital charges (in US dollars).

RESULTS

A total of 141,007 ACDF operations were identified. IONM was used in 9540 cases (6.8%). No significant association was found between neurological complications and use of IONM on univariate analysis (OR 0.80, p = 0.39) or multivariate regression (OR 0.82, p = 0.45). By contrast, age ≥ 65 years, multilevel fusion, CCI score > 0, and a nonelective admission were associated with greater incidence of neurological complication. The propensity score–matched cohort consisted of 18,760 patients who underwent ACDF with (n = 9380) or without (n = 9380) IONM. Rates of neurological complication were comparable between IONM and non-IONM (0.17% vs 0.22%, p = 0.41) groups. IONM and non-IONM groups had a comparable proportion of patients with LOS ≥ 2 days (19% vs 18%, p = 0.15). The use of IONM was associated with an additional $6843 (p < 0.01) in hospital charges.

CONCLUSIONS

The use of IONM was not associated with a reduced rate of neurological complications following ACDF. Limitations of the data source precluded a specific assessment of the effectiveness of IONM in preventing neurological complications in patients with more complex pathology (i.e., ossification of the posterior longitudinal ligament or cervical deformity).

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Michael P. Kelly, Lawrence G. Lenke, Jakub Godzik, Ferran Pellise, Christopher I. Shaffrey, Justin S. Smith, Stephen J. Lewis, Christopher P. Ames, Leah Y. Carreon, Michael G. Fehlings, Frank Schwab and Adam L. Shimer

OBJECTIVE

The authors conducted a study to compare neurological deficit rates associated with complex adult spinal deformity (ASD) surgery when recorded in retrospective and prospective studies. Retrospective studies may underreport neurological deficits due to selection, detection, and recall biases. Prospective studies are expensive and more difficult to perform, but they likely provide more accurate estimates of new neurological deficit rates.

METHODS

New neurological deficits were recorded in a prospective study of complex ASD surgeries (pSR1) with a defined outcomes measure (decrement in American Spinal Injury Association lower-extremity motor score) for neurological deficits. Using identical inclusion criteria and a subset of participating surgeons, a retrospective study was created (rSR1) and neurological deficit rates were collected. Continuous variables were compared with the Student t-test, with correction for multiple comparisons. Neurological deficit rates were compared using the Mantel-Haenszel method for standardized risks. Statistical significance for the primary outcome measure was p < 0.05.

RESULTS

Overall, 272 patients were enrolled in pSR1 and 207 patients were enrolled in rSR1. Inclusion criteria, defining complex spinal deformities, and exclusion criteria were identical. Sagittal Cobb measurements were higher in pSR1, although sagittal alignment was similar. Preoperative neurological deficit rates were similar in the groups. Three-column osteotomies were more common in pSR1, particularly vertebral column resection. New neurological deficits were more common in pSR1 (pSR1 17.3% [95% CI 12.6–22.2] and rSR1 9.0% [95% CI 5.0–13.0]; p = 0.01). The majority of deficits in both studies were at the nerve root level, and the distribution of level of injury was similar.

CONCLUSIONS

New neurological deficit rates were nearly twice as high in the prospective study than the retrospective study with identical inclusion criteria. These findings validate concerns regarding retrospective cohort studies and confirm the need for and value of carefully designed prospective, observational cohort studies in ASD.

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Shian Liu, Renaud Lafage, Justin S. Smith, Themistocles S. Protopsaltis, Virginie C. Lafage, Vincent Challier, Christopher I. Shaffrey, Kris Radcliff, Paul M. Arnold, Jens R. Chapman, Frank J. Schwab, Eric M. Massicotte, S. Tim Yoon, Michael G. Fehlings and Christopher P. Ames

OBJECT

Cervical stenosis is a defining feature of cervical spondylotic myelopathy (CSM). Matsunaga et al. proposed that elements of stenosis are both static and dynamic, where the dynamic elements magnify the canal deformation of the static state. For the current study, the authors hypothesized that dynamic changes may be associated with myelopathy severity and neck disability. This goal of this study was to present novel methods of dynamic motion analysis in CSM.

METHODS

A post hoc analysis was performed of a prospective, multicenter database of patients with CSM from the AOSpine North American study. One hundred ten patients (34%) met inclusion criteria, which were symptomatic CSM, age over 18 years, baseline flexion/extension radiographs, and health-related quality of life (HRQOL) questionnaires (modified Japanese Orthopaedic Association [mJOA] score, Neck Disability Index [NDI], the 36-Item Short Form Health Survey Physical Component Score [SF-36 PCS], and Nurick grade). The mean age was 56.9 ± 12 years, and 42% of patients were women (n = 46). Correlations with HRQOL measures were analyzed for regional (cervical lordosis and cervical sagittal vertical axis) and focal parameters (kyphosis and spondylolisthesis between adjacent vertebrae) in flexion and extension. Baseline dynamic parameters (flexion/extension cone relative to a fixed C-7, center of rotation [COR], and range of motion arc relative to the COR) were also analyzed for correlations with HRQOL measures.

RESULTS

At baseline, the mean HRQOL measures demonstrated disability and the mean radiographic parameters demonstrated sagittal malalignment. Among regional parameters, there was a significant correlation between decreased neck flexion (increased C2–7 angle in flexion) and worse Nurick grade (R = 0.189, p = 0.048), with no significant correlations in extension. Focal parameters, including increased C-7 sagittal translation overT-1 (slip), were significantly correlated with greater myelopathy severity (mJOA score, Flexion R = −0.377, p = 0.003; mJOA score, Extension R = −0.261, p = 0.027). Sagittal slip at C-2 and C-4 also correlated with worse HRQOL measures. Reduced flexion/extension motion cones, a more posterior COR, and smaller range of motion correlated with worse general health SF-36 PCS and Nurick grade.

CONCLUSIONS

Dynamic motion analysis may play an important role in understanding CSM. Focal parameters demonstrated a significant correlation with worse HRQOL measures, especially increased C-7 sagittal slip in flexion and extension. Novel methods of motion analysis demonstrating reduced motion cones correlated with worse myelopathy grades. More posterior COR and smaller range of motion were both correlated with worse general health scores (SF-36 PCS and Nurick grade). To our knowledge, this is the first study to demonstrate correlation of dynamic motion and listhesis with disability and myelopathy in CSM.

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Dominic Maggio, Tamir T. Ailon, Justin S. Smith, Christopher I. Shaffrey, Virginie Lafage, Frank Schwab, Regis W. Haid Jr., Themistocles Protopsaltis, Eric Klineberg, Justin K. Scheer, Shay Bess, Paul M. Arnold, Jens Chapman, Michael G. Fehlings, Christopher Ames, AOSpine North America and International Spine Study Group

OBJECT

The associations among global spinal alignment, patient-reported disability, and surgical outcomes have increasingly gained attention. The assessment of global spinal alignment requires standing long-cassette anteroposterior and lateral radiographs; however, spine surgeons routinely rely only on short-segment imaging when evaluating seemingly isolated lumbar pathology. This may prohibit adequate surgical planning and may predispose surgeons to not recognize associated pathology in the thoracic spine and sagittal spinopelvic malalignment. The authors used a case-based survey questionnaire to evaluate if including long-cassette radiographs led to changes to respondents' operative plans as compared with their chosen plan when cases contained standard imaging of the involved lumbar spine only.

METHODS

A case-based survey was distributed to AOSpine International members that consisted of 15 cases of lumbar spine pathology and lumbar imaging only. The same 15 cases were then shuffled and presented a second time with additional long-cassette radiographs. Each case required participants to select a single operative plan with 5 choices ranging from least to most extensive. The cases included 5 “control” cases with normal global spinal alignment and 10 “test” cases with significant sagittal and/or coronal malalignment. Mean scores were determined for each question with higher scores representing more invasive and/or extensive operative plans.

RESULTS

Of 712 spine surgeons who started the survey, 316 (44%) completed the entire series, including 68% of surgeons with spine fellowship training and representation from more than 40 countries. For test cases, but not for control cases, there were significantly higher average surgical invasiveness scores for cases presented with long-cassette radiographs (4.2) as compared with those cases with lumbar imaging only (3.4; p = 0.002). The addition of long-cassette radiographs resulted in 82.1% of respondents recommending instrumentation up to the thoracic spine, a 23.2% increase as compared with the same cases presented with lumbar imaging only (p = 0.008).

CONCLUSIONS

This study demonstrates the importance of maintaining a low threshold for performing standing long-cassette imaging when assessing seemingly isolated lumbar pathology. Such imaging is necessary for the assessment of spinopelvic and global spinal alignment, which can be important in operative planning. Deformity, particularly positive sagittal malalignment, may go undetected unless one maintains a high index of suspicion and obtains long-cassette radiographs. It is recommended that spine surgeons recognize the prevalence and importance of such deformity when contemplating operative intervention.

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Robert G. Grossman, Ralph F. Frankowski, Keith D. Burau, Elizabeth G. Toups, John W. Crommett, Michele M. Johnson, Michael G. Fehlings, Charles H. Tator, Christopher I. Shaffrey, Susan J. Harkema, Jonathan E. Hodes, Bizhan Aarabi, Michael K. Rosner, James D. Guest and James S. Harrop

Object

The aim of this multicenter, prospective study was to determine the spectrum, incidence, and severity of complications during the initial hospitalization of patients with spinal cord injury.

Methods

The study was conducted at 9 university-affiliated hospitals that comprise the clinical centers of the North American Clinical Trials Network (NACTN) for Treatment of Spinal Cord Injury. The study population comprised 315 patients admitted to NACTN clinical centers between June 25, 2005, and November 2, 2010, who had American Spinal Injury Association (ASIA) Impairment Scale grades of A–D and were 18 years of age or older. Patients were managed according to a standardized protocol.

Results

The study population was 79% male with a median age of 44 years. The leading causes of injury were falls (37%) and motor vehicle accidents (28%). The distribution of initial ASIA grades were A (40%), B (16%), C (15%), and D (29%). Fifty-eight percent of patients sustained 1 or more severe, moderate, or mild complications. Complications were associated with more severe ASIA grade: 84% of patients with Grade A and 25% of patients with Grade D had at least 1 complication. Seventy-eight percent of complications occurred within 14 days of injury. The most frequent types of severe and moderate complications were respiratory failure, pneumonia, pleural effusion, anemia, cardiac dysrhythmia, and severe bradycardia. The mortality rate was 3.5% and was associated with increased age and preexisting morbidity.

Conclusions

Knowledge of the type, frequency, time of occurrence, and severity of specific complications that occur after spinal cord injury can aid in their early detection, treatment, and prevention. The data are of importance in evaluating and selecting therapy for clinical trials.