Accepted Manuscript Somatosensory evoked potential monitoring during instrumented scoliosis corrective procedures: validity revisited Parthasarathy Thirumala, MD Lance Bodily, BS Derrick Tint, BS W. Timothy Ward, MD Vincent F. Deeney, MD Donald Crammond, PhD Miguel E. Habeych, MD, MPH Jeffrey Blazer, PhD PII:
S1529-9430(13)01575-1
DOI:
10.1016/j.spinee.2013.09.035
Reference:
SPINEE 55580
To appear in:
The Spine Journal
Received Date: 26 October 2012 Revised Date:
16 August 2013
Accepted Date: 19 September 2013
Please cite this article as: Thirumala P, Bodily L, Tint D, Ward WT, Deeney VF, Crammond D, Habeych ME, Blazer J, Somatosensory evoked potential monitoring during instrumented scoliosis corrective procedures: validity revisited, The Spine Journal (2013), doi: 10.1016/j.spinee.2013.09.035. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Somatosensory evoked potential monitoring during instrumented scoliosis corrective procedures: validity revisited.
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Parthasarathy Thirumala, MD Department of Neurological Surgery
UPMC Presbyterian Suite B-400
200 Lothrop Street
Pittsburgh, PA 15213 Phone: (412) 648-2570
[email protected] W. Timothy Ward, MD UPMC, Orthopedic Surgery Pittsburgh, PA
Donald Crammond, PhD UPMC, Neurosurgey Pittsburgh, PA
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Miguel Habeych, MD, MPH UPMC, Neurosurgey Pittsburgh, PA
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Vincent F. Deeney, MD UPMC, Orthopedic Surgery Pittsburgh, PA
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Derrick Tint, BS University of Pittsburgh School of Medicine Pittsburgh, PA
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Lance Bodily, BS University of Pittsburgh School of Medicine Pittsburgh, PA
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Jeffrey Blazer, PhD UPMC, Neurosurgey Pittsburgh, PA
Key Words: Scoliosis; Somatosensory evoked potential; Transcranial motor evoked potential Word Count: 4,355
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Somatosensory evoked potential monitoring during instrumented scoliosis
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corrective procedures: Utility revisited.
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Abstract:
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Background: Intraoperative monitoring (IOM) using somatosensory evoked
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potentials (SSEP's) plays an important role in reducing iatrogenic neurological
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deficits during corrective pediatric idiopathic scoliosis procedures. However, for
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unknown reasons recent reports have cited that the sensitivity of SSEPs to detect
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neurological deficits has decreased, in some to be less than 50%. This current trend,
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which is coincident with the addition of transcranial electrical motor evoked
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potentials (tceMEP's), is surprising given that SSEPs are robust, reproducible
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responses that were previously shown to have sensitivity and specificity of >90%.
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Purpose: Our primary aim was to assess whether SSEPs alone can detect impending
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neurological deficits with similar sensitivity and specificity as originally reported.
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Our secondary aim was to estimate the potential predictive value of adding
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tceMEP's to SSEP's monitoring in idiopathic scoliosis procedures.
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Design: This was a retrospective review to analyze the efficacy of SSEP monitoring
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in the group of pediatric instrumented scoliosis cases.
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Patient sample: We retrospectively reviewed all consecutive cases of patients who
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underwent idiopathic scoliosis surgery between 1999 and 2009 at Children's
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Hospital of Pittsburgh. We identified 477 patients who had the surgery with SSEP
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monitoring alone. Exclusion criteria included any patients with neuromuscular
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disorders or unreliable SSEP monitoring. Patients who had incomplete
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neurophysiology data or incomplete postoperative records were also excluded.
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Outcome measures:Major outcomes measured were clinically significant
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postoperative sensory or motor deficits, as well as significant intraoperative SSEP
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changes.
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Methods: Continuous interleaved upper and lower extremity SSEP's were obtained
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throughout the duration of all procedures. We considered a persistent 50%
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reduction in primary somatosensory cortical amplitude or a prolongation of
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response latency by >10% from baseline to be significant. Persistent changes
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represent significant deviation in SSEP amplitude or latency in more than two
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consecutive averaged trials. Patients were classified into one of four categories with
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respect to SSEP monitoring: true positive, false positive, true negative, and false
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negative. The sensitivity, specificity, positive predictive value (PPV) and negative
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predictive value (NPV) were then calculated accordingly.
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Results: Our review of 477 idiopathic scoliosis surgeries monitored using SSEP's
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alone revealed a new deficit rate of 0.63% with no cases of permanent injury.
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Sensitivity=95.0%, specificity=99.8%, PPV=95%, NPV=99.8%. Using evidence-
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based epidemiological measures, we calculated that the number needed to treat
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(NNT) was 1,587 patients for one intervention to be performed that would have
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been missed by SSEP monitoring alone. Additionally, the number needed to harm,
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which represents the increase in false positives with the addition of tceMEP's, was
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200.
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Conclusion: SSEP monitoring alone during idiopathic scoliosis continues to be a
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highly reliable method for the detection and prevention of iatrogenic injury. Our
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results confirm the high sensitivity and specificity of SSEP monitoring alone
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published in earlier literature. As such, we suggest the continued use of SSEP alone
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in idiopathic scoliosis surgeries. At this time we do not believe there is sufficient
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data to support the addition of MEP monitoring, although further studies and
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revised criteria for the use of MEP may provide added value for its use in the future.
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Intro: For pediatric patients with severe scoliosis, instrumented spinal fusions are
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essential to halt progression and ameliorate symptoms. Iatrogenic injury during
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scoliosis procedures can occur, most often related to derotation of the spinal column
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causing direct injury to the spinal cord or impinging on the vasculature1. While the
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incidence of iatrogenic spinal cord injury resulting in paraplegia is low, this is a
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feared complication as the patients are generally young and otherwise healthy.
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Intraoperative monitoring (IOM) using somatosensory evoked potentials (SSEP)
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plays an important role in reducing iatrogenic neurological deficits during these
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corrective scoliosis procedures. A large multi center study reported a reduction of
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persistent and major persistent neurological deficits to decrease from 0.72%
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without monitoring to 0.55% with SSEP monitoring2. The most recent reports cite
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total neurological deficits from scoliosis surgery, the sum of transient and persistent
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deficits, to be 0.99% and 1.84% for pediatric and adult patients respectively. Lower
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incidence rates were reported in idiopathic cases having rates of 0.73% and 1.45%
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for pediatric and adult patients respectively3.
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Multiple research studies have reported that addition of transcranial motor evoked
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potential (TcMEP) monitoring to SSEPs increases the sensitivity of IOM significantly,
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during scoliosis surgery. Many of these studies conclude that TcMEP is a better
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assay of the motor tracts, and suggest that it has greater efficacy in preventing
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motor deficits4,5. Moreover, for reasons that are unclear, the reported sensitivity of
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SSEPs to detect a neurological deficit has decreased from close to 100% in large
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studies 2,6 to less than 50%4,5,7 in more recent studies over the last decade. This new
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development is surprising given that SSEPs provide robust responses that were
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previously shown to be highly sensitive and specific1,2_ENREF_1. In addition,
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TcMEPs lack well-defined and accepted alarm criteria to alert the surgeon about an
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impending neurological deficit. Our primary aim is to assess whether SSEP alone
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can detect impending neurological deficits with similar sensitivity and specificity as
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previously reported. We also try to determine the potential need and value of
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additional monitoring with TcMEPs, considering the current alarm criteria being
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used by the field.
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Materials and Methods
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Study Design
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We retrospectively reviewed consecutive cases of patients who underwent scoliosis
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surgery for idiopathic and congenital scoliosis between 1999 and 2009. We
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identified 477 patients who had the surgery with SSEP monitoring. These
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procedures were performed by the same surgeons (WTW, VD, JSG, SAM) at UPMC
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Children’s Hospital.
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Inclusion criteria included all patients with idiopathic and congenital scoliosis
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undergoing instrumented spinal fusions for scoliosis correction. Exclusion criteria
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included any patients with neuromuscular disorders (neurogenic scoliosis) or
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abnormal baseline SSEP signals that did not allow monitoring. Patients who had
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incomplete neurophysiology data or incomplete postoperative records were also
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excluded.
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Neurophysiologic Monitoring:
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Intraoperative SSEP monitoring is standard at our institution for all instrumented
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spinal fusions of scoliosis patients based on its documented efficacy1. Baseline SSEP
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values were obtained after the induction of anesthesia but before patient
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positioning in all cases. Continuous upper and lower extremity interleaved SSEPs
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were obtained throughout the procedure. Physician oversight and interpretation
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was performed using a combined on-site and remote model implemented at UPMC.
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In all cases, a board-certified Neurophysiologist (American Board of
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Neurophysiological Monitoring) was on-site, in person available for interpretation
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while physician (neurologists) oversight, supervision, and interpretation were
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performed in-person on-site or remotely. The oversight physician provided
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supervision to 4-5 cases simultaneously on average with a maximum of 8 cases.
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Upper Extremity SSEPs:
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Median or ulnar nerve stimulation was performed bilaterally in an alternating
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fashion at the wrist with sub dermal needle electrode pairs. P4/Fz and P3/Fz scalp
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electrodes montages were used (per the international 10–20 system) for recording
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cortically generated responses. A cervical electrode was localized at the C7 spinous
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process or mastoid (M) and referenced to Fz was used for subcortical recordings.
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Stimulation frequency was 2.45 Hz with duration of 0.2 milliseconds. Band pass
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filters were set at 10 to 300 Hz with a gain of 20k for cortical recordings and 30 to
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1,000 Hz for subcortical recordings with a gain of 50K. Averages were computed for
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either 128 or 256 trials, depending on the signal to noise ratio.
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Lower Extremity SSEPs.
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For the lower extremities, bilateral alternating tibial nerve stimulation was used.
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Peroneal nerve stimulation was used when high quality tibial nerve responses could
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not be elicited. Tibial nerve stimulation was performed at the medial malleolus of
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the ankle with sub dermal needle electrode pairs with a proximally placed cathode
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and an anode placed approximately 1 cm distally. The peroneal nerve was
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stimulated using pairs of sub dermal needles located at the head of the fibula and
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medially in the popliteal fossa. Recordings were obtained from the scalp and
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cervical region with subdermal electrodes. Pz/Fz and P4/P3 scalp electrodes
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montages were used (per the international 10–20 system) for recording cortical
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potentials. A cervical electrode was localized at the C7 spinous process or at the
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level of the mastoid and referenced to Fz was used for subcortical potentials.
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Stimulation frequency was 2.45 Hz with duration of 0.2 milliseconds. Band pass
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filters were set at 30 to 300 Hz for cortical recordings and 30 to 1,000 Hz for
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cervical recordings. Averages were computed for either 128 or 256 trials depending
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on the signal quality. IOM for the procedures in this study did not involve
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transcranial motor evoked potentials (TcMEPs) or stimulus triggered EMG
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recording in response to pedicel screw stimulation.
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Anesthesia:
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General anesthesia with inhalation agents (1 MAC or less) and adjunct intravenous
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agents were used for all patients. Muscle relaxants were used during induction and
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maintained throughout the procedure.
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Alarm Criteria:
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The initial recordings made after induction of anesthesia and before positioning were used as baseline potentials. Continuous SSEP signal averages were collected.
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We considered a persistent, 50% reduction in primary somatosensory cortical
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amplitude or a prolongation of response latency by >10% from baseline to be
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significant. “Persistent changes” represent changes in amplitude or latency of the
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SSEPs in more than two averaged trials. The primary reason for using more than 2
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trials is to eliminate technical issues like noise as the reason for the change. These
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criteria are generally agreed on in the literature as being of optimal sensitivity and
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specificity for detecting iatrogenic spinal cord injury8-10. Henceforth, these
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threshold signal changes will be referred to as “significant.”
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Record Review:
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The preoperative and postoperative charts of all patients were examined and
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compared to assess the presence of a new neurological injury. All motor, sensory,
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bowel, or bladder symptoms of new onset were considered to be iatrogenic in
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nature. This assessment was performed blinded to the neurophysiology data. A
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new motor, sensory, bowel or bladder deficit is defined as a change in the
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neurological status of the patient as noted in the chart in the progress note,
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consultant note, and or discharge notes when compared to their preoperative
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neurological condition. The neurophysiology data was examined in conjunction
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with neurophysiology technologist notes to assess all cases in which a significant
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change in waveforms occurred. This assessment was performed blinded to the
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medical charts documenting postoperative neurological status. For those cases in
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which a significant change was observed, examination of the technician notes/data
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was performed to correlate the change, if possible, with the corresponding
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procedural cause—instrumentation, hypotension, positioning, correction of the
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deformity—as well as the intervention performed, if any, to correct the changes in
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signals and whether or not the signals returned. The medical charts were reviewed
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to assess the neurological status of the patient post-operatively, upon discharge, and
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at follow up. Transient deficits were defined as those that were observed post-
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operatively but had resolved at discharge or subsequent visits with the duration for
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recovery noted. Permanent deficits were defined as those that were not resolved at
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discharge or subsequent follow up. The most recent long-term follow-up
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appointment was also reviewed, with an average follow-up of 4.4 years.
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Data Analysis:
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To obtain diagnostic test statistics significant changes were classified as true
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positive (TP), false positive (FP), true negative (TN), or false negative (FN) with the
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following criteria:
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TP: Significant SSEP signal changes accompanied by a new postoperative neurologic
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deficit; or, a case where significant SSEP signal deterioration occurred as the result
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of a recognized intraoperative cause, event or complication; or, a case where a
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significant SSEP signal deterioration improved to baseline value after a specific
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intraoperative intervention.
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TN: Normal intraoperative SSEP signals in the absence of new postoperative deficits.
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FP: persistent significant SSEP signal deterioration, which did not improve with
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intraoperative interventions and the patient, woke up neurologically intact.
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FN: Normal intraoperative SSEP signals with a new postoperative neurologic deficit.
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Results:
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Demographic information:
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Age:
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The average age of the patients overall was 14 years old, with a range from 1-28
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years old. 41 patients were between the age of 1-10 years old, 404 patients were
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between the ages of 11-18 years old, 31 patients were between the ages of 19-25
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years old, and one patient was 28 years old.
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Among those with significant IONM changes, the average age was 14.5 years old. Of
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patients with significant IONM changes, 19 were between the ages of 11-18 and one
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was between the ages of 19-25 years old.
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Of the 3 patients with new post-operative deficits the average age was 18 years old
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with ages of 16, 22, and 16.
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Sex:
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There were 352 females and 125 males in this series, for 74% and 26% of the series
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respectively.
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Among the 20 patients with significant IONM changes, 14 were female and 6 were
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males, 70% and 30% respectively.
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Among the 3 patients with postoperative deficits 1 was male and 2 were female,
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33% and 66% respectively.
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Operative Date:
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Overall 120 cases were performed between 6/14/99-7/8/03 (group 1), 120 cases
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between 7/10/03-3/17/05 (group 2), 119 cases between 3/17/05-7/10/07 (group
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3) and 118 cases between 7/12/07-3/12/09 (group 4).
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Among the 20 cases with significant changes, 9 correspond to group one, 3 to group
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2, 6 to group 3, and 2 to group 4.
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Of the 3 patients with post-operative deficits, 2 correspond to group 1, 0 to group 2,
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1 to group 3, and 0 to group 4.
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3 Post operative deficits and SSEP changes (table 1):
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The incidence of significant SSEP change was 20/477 (4.2%). The incidence of new
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postoperative deficits was 3/477 (0.63%) (table 1). The incidence of new
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postoperative deficit in patients who had changes in SSEPs was 2/477 (0.42%).
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Although patient 3 did have changes in SSEPs, they were not clearly correlated with
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the deficit. This resulted in 1/477 (0.21%) of patients with a post-operative
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neurological deficit without changes in SSEPs. The incidence of serious and
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permanent neurological injury was 0/477 (0.00%).
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True Positives:
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19/477 cases were determined to be true positives as they were observed to have
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significant changes in intraoperative SSEP monitoring associated with a clear
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surgical cause. This allowed an intervention to be made that resulted in the return
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of the signals to baseline or resulted in a deficit. As the discussion above indicates,
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the lack of correlation between the deficit and SSEP changes in patient 3 compels us
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to classify this patient as both a false positive and false negative rather than a true
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positive.
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Clinical context of SSEP changes (table 3):
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As outlined in table 3 below 10/19 of these changes were related to instrumentation,
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5/19 were related to hypotensive episodes, 3/19 were related to poor positioning,
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and 1/19 was related to a tight blood pressure cuff.
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Rod placement (n=5): Patients 2, 4, 7, 8, 9 had SSEP changes associated with rod
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placement and subsequent derotation. In patients 2,4,7,8, and 9 adjustment of the
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rods led to return of the SSEP responses and were not associated with a
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postoperative deficit.
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Wire Tightening (n=3): Patients 10, 14*, and 16 had SSEP changes associated with
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tightening of sub laminar wires. In patients 10 and 16 loosening of the wires was
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associated with return of the SSEP responses and no postoperative deficit. In
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patient 14 the SSEP responses improved to a degree but remained poor relative to
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baseline for an extended period of time before returning to baseline at the end of the
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procedure. The patient subsequently woke up with left sided weakness of the upper
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and lower extremities.
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Hook Placement (n=1): Patient 18 had deterioration of SSEP responses associated
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with placement of hooks. Removal and replacement resulted in the responses
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returning to baseline. No new postoperative deficit was observed.
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Removal of old instrumentation (n=1): Patient 6 was undergoing a PSF revision and
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had a deterioration of SSEP signals with removal of his old instrumentation.
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However, the signal soon returned to baseline and no deficit was observed.
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Poor Patient Positioning (n=3): Patients 17*, 19, and 20 had SSEP changes that were
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correlated with poor positioning. 19 and 20 had their SSEP signals return fully to
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baseline with adjustment of positioning and did not have postoperative deficits.
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While patient 17 had some improvement of SSEP signals with adjustment of
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positioning, they remained poor relative to his preoperative baseline throughout the
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procedure.
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Hypotension (n=5): Patients 1, 11, 12, 13, 15 all experienced hypotensive (less than
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or equal to 60mmHg MAP) episodes intraoperatively that were associated with
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changes in SSEP signals. All of these SSEP changes resolved after increasing the
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MAP and none were associated with a postoperative deficit.
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Tight Pressure cuff (n=1): Patient 5 had a poor upper right extremity response that
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was thought to be associated with a tight blood pressure cuff. Once removed the
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signals returned to baseline and the patient did not have a deficit postoperatively.
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Clinical context of patients with SSEP changes and deficits (table 2):
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Patient 14 was a 23yr old woman with kyphoscoliosis who, during the course of
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instrumentation, had complete loss of bilateral peroneal nerve SSEPs. These
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responses improved when the instrumentation wires were loosened and returned
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to baselines at the end of the procedure. The patient awoke with a motor deficit,
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which at the time of discharge had improved to 2/5 strength in the left leg and 3/5
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in the right leg. Her deficit had fully resolved, with 5/5 strength in upper and lower
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extremities at 3 month follow up.
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Patient 17 was 14yr old boy who had changes in the right median nerve cortical and
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subcortical responses. This was believed to be secondary to positioning of the
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patient. He had right upper extremity weakenss (3/5)in the wrist flexor, extensor,
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finger flexor, extensor muscles. He improved to a 5/5 power in the right upper
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extremity before discharge.
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False Positive and False negative:
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Patient 3 was a 17yr old girl who showed loss of her left tibial nerve SSEPs during
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rod placement. A subsequent test of peroneal nerve SSEP indicated a presence of a
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good cortical response. A wake up test was performed intraoperatively and the
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patient moved all four extremities. The tibial response recovered and was at
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baseline values at closure. The patient however woke up with a post-operative
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deficit that was observed to be in the distribution of the musculocutaneous nerve.
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True Negatives:
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We had a total of 457/477 (95.8 %) patients who had no changes in intraoperative
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monitoring and no neurological deficit.
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Statistical analysis:
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All the 477 patients were classified into one of the four categories (TP, FP, TN, FN)
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as described in the data analysis and a (2x2) table was thus created. The sensitivity,
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specificity, positive predictive value and negative predictive value then calculated
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accordingly (table 4).
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This results in the following test statistics for SSEP monitoring: sensitivity=
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19/20=95.0%, specificity= 457/458=99.8%, PPV= 19/20=95%,
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NPV=457/458=99.8%.
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True positive rate 19/477= 3.98%; False positive rate 1/477= 0.21%; True negative
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rate 457/477= 95.8%; False negative rate 1/477= 0.21%.
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Discussion
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The results of our instrumented scoliosis procedures monitored with SSEP alone
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reveal a total injury rate of 0.63% and a permanent deficit rate of 0.00%. SSEP
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monitoring alone was observed to have 95.0% sensitivity and 99.8% specificity.
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Our results for iatrogenic injury are slightly lower than, but consistent with, the
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most recent rates of total injury and persistent/serious injury rate for idiopathic
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scoliosis procedures in the literature1-3. Of the deficits that occurred during this
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series all resolved within days to weeks. Significant changes in SSEP responses
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were observed in 20 cases (4.2%), with 19/20 (95.0%) being true positives. This is
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similar to other reports in the literature2,3_ENREF_2. As table 3 outlines, 10/20
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changes were due to instrumentation, 5/20 were the result of hypotension during
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surgery, 3/20 were the result of poor patient positioning, and one was the result of a
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tight blood pressure cuff with distal extremity ischemia.
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The majority of SSEP changes in this series were related to insertion, adjustment, or
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removal of the instrumentation used during correction of the scoliotic deformity.
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Placement of instrumentation involves corrective rods, wires, screws, and hooks, as
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well as manual tightening of these instruments to achieve some correction of the
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spinal column and to prevent further deformation1,2. Placement of instrumentation
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and subsequent derotation can result in impingement on the vasculature of the
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spinal cord or direct compression of the neural structures, resulting in ischemia1,2.
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Animal studies have confirmed that a significant loss of SSEP responses results from
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“electrical failure” of the neural structures. This change precedes “ion pump failure”
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and ensuing infarction. Timely intervention during the critical window between
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electrical and ion pump failure can prevent permanent neurological deficits11. In
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9/10 of the cases involving changes related to instrumentation, immediate
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interventions resulted in return of the SSEP signals to baseline with no
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postoperative deficit in our study. However, in 1 case the patient’s responses were
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slow to return and the patient experienced a transient deficit that resolved in
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approximately 1 month. Collectively this data would suggest that SSEP monitoring
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aided in avoiding several postoperative deficits and may have helped in reducing
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the severity of the deficits that did occur, as has been suggested in prior studies12.
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Low MAP (