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C. Rory Goodwin, Eric W. Sankey, Ann Liu, Benjamin D. Elder, Thomas Kosztowski, Sheng-Fu L. Lo, Charles G. Fisher, Michelle J. Clarke, Ziya L. Gokaslan, and Daniel M. Sciubba

OBJECT

Surgical procedures and/or adjuvant therapies are effective modalities for the treatment of symptomatic spinal metastases. However, clinical results specific to the skin cancer spinal metastasis cohort are generally lacking. The purpose of this study was to systematically review the literature for treatments, clinical outcomes, and survival following the diagnosis of a skin cancer spinal metastasis and evaluate prognostic factors in the context of spinal skin cancer metastases stratified by tumor subtype.

METHODS

The authors performed a literature review using PubMed, Embase, CINAHL, and Web of Science to identify articles since 1950 that reported survival, clinical outcomes, and/or prognostic factors for the skin cancer patient population with spinal metastases. The methodological quality of reviews was assessed using the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) tool.

RESULTS

Sixty-five studies met the preset criteria and were included in the analysis. Of these studies, a total of 25, 40, 25, and 12 studies included patients who underwent some form of surgery, radiotherapy, chemotherapy, or observation alone, respectively. Sixty-three of the 65 included studies were retrospective in nature (Class of Evidence [CoE] IV), and the 2 prospective studies were CoE II. Based on the studies analyzed, the median overall survival for a patient with a spinal metastasis from a primary skin malignancy is 4.0 months; survival by tumor subtype is 12.5 months for patients with basal cell carcinoma (BCC), 4.0 months for those with melanoma, 4.0 months for those with squamous cell carcinoma, 3.0 months for those with pilomatrix carcinoma, and 1.5 months for those with Merkel cell carcinoma (p < 0.0001). The overall percentage of known continued disease progression after spine metastasis diagnosis was 40.1% (n = 244/608, range 25.0%–88.9%), the rate of known recurrence of the primary skin cancer lesion was 3.5% (n = 21/608, range 0.2%–100.0%), and the rate of known spine metastasis recurrence despite treatment for all skin malignancies was 2.8% (n = 17/608, range 0.0%–33.3%). Age greater than 65 years, sacral spinal involvement, presence of a neurological deficit, and nonambulatory status were associated with decreased survival in patients diagnosed with a primary skin cancer spinal metastasis. All other clinical or prognostic parameters were of low or insufficient strength.

CONCLUSIONS

Patients diagnosed with a primary skin cancer metastasis to the spine have poor overall survival with the exception of those with BCC. The median duration of survival for patients who received surgical intervention alone, medical management (chemotherapy and/or radiation) alone, or the combination of therapies was similar across interventions. Age, spinal region, and neurological status may be associated with poor survival following surgery.

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Zach Pennington, Daniel Lubelski, Erick M. Westbroek, A. Karim Ahmed, Jeff Ehresman, Matthew L. Goodwin, Sheng-Fu Lo, Timothy F. Witham, Ali Bydon, Nicholas Theodore, and Daniel M. Sciubba

OBJECTIVE

Postoperative C5 palsy affects 7%–12% of patients who undergo posterior cervical decompression for degenerative cervical spine pathologies. Minimal evidence exists regarding the natural history of expected recovery and variables that affect palsy recovery. The authors investigated pre- and postoperative variables that predict recovery and recovery time among patients with postoperative C5 palsy.

METHODS

The authors included patients who underwent posterior cervical decompression at a tertiary referral center between 2004 and 2018 and who experienced postoperative C5 palsy. All patients had preoperative MR images and full records, including operative note, postoperative course, and clinical presentation. Kaplan-Meier survival analysis was used to evaluate both times to complete recovery and to new neurological baseline—defined by deltoid strength on manual motor testing of the affected side—as a function of clinical symptoms, surgical maneuvers, and the severity of postoperative deficits.

RESULTS

Seventy-seven patients were included, with an average age of 64 years. The mean follow-up period was 17.7 months. The mean postoperative C5 strength was grade 2.7/5, and the mean time to first motor examination with documented C5 palsy was 3.5 days. Sixteen patients (21%) had bilateral deficits, and 9 (12%) had new-onset biceps weakness; 36% of patients had undergone C4–5 foraminotomy of the affected root, and 17% had presented with radicular pain in the dermatome of the affected root. On univariable analysis, patients’ reporting of numbness or tingling (p = 0.02) and a baseline deficit (p < 0.001) were the only predictors of time to recovery. Patients with grade 4+/5 weakness had significantly shorter times to recovery than patients with grade 4/5 weakness (p = 0.001) or ≤ grade 3/5 weakness (p < 0.001). There was no difference between those with grade 4/5 weakness and those with ≤ grade 3/5 weakness. Patients with postoperative strength < grade 3/5 had a < 50% chance of achieving complete recovery.

CONCLUSIONS

The timing and odds of recovery following C5 palsy were best predicted by the magnitude of the postoperative deficit. The use of C4–5 foraminotomy did not predict the time to or likelihood of recovery.

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Xuguang Chen, Sheng-Fu L. Lo, Chetan Bettegowda, Daniel M. Ryan II, John M. Gross, Chen Hu, Lawrence Kleinberg, Daniel M. Sciubba, and Kristin J. Redmond

OBJECTIVE

Spinal chordoma is locally aggressive and has a high rate of recurrence, even after en bloc resection. Conventionally fractionated adjuvant radiation leads to suboptimal tumor control, and data regarding hypofractionated regimens are limited. The authors hypothesized that neoadjuvant stereotactic body radiotherapy (SBRT) may overcome its intrinsic radioresistance, improve surgical margins, and allow preservation of critical structures during surgery. The purpose of this study is to review the feasibility and early outcomes of high-dose hypofractionated SBRT, with a focus on neoadjuvant SBRT.

METHODS

Electronic medical records of patients with spinal chordoma treated using image-guided SBRT between 2009 and 2019 at a single institution were retrospectively reviewed.

RESULTS

Twenty-eight patients with 30 discrete lesions (24 in the mobile spine) were included. The median follow-up duration was 20.8 months (range 2.3–126.3 months). The median SBRT dose was 40 Gy (range 15–50 Gy) in 5 fractions (range 1–5 fractions). Seventeen patients (74% of those with newly diagnosed lesions) received neoadjuvant SBRT, of whom 15 (88%) underwent planned en bloc resection, all with negative margins. Two patients (12%) developed surgical wound-related complications after neoadjuvant SBRT and surgery, and 4 (two grade 3 and two grade 2) experienced postoperative complications unrelated to the surgical site. Of the remaining patients with newly diagnosed lesions, 5 received adjuvant SBRT for positive or close surgical margins, and 1 received SBRT alone. Seven recurrent lesions were treated with SBRT alone, including 2 after failure of prior conventional radiation. The 2-year overall survival rate was 92% (95% confidence interval [CI] 71%–98%). Patients with newly diagnosed chordoma had longer median survival (not reached) than those with recurrent lesions (27.7 months, p = 0.006). The 2-year local control rate was 96% (95% CI 74%–99%). Among patients with radiotherapy-naïve lesions, no local recurrence was observed with a biologically effective dose ≥ 140 Gy, maximum dose of the planning target volume (PTV) ≥ 47 Gy, mean dose of the PTV ≥ 39 Gy, or minimum dose to 80% of the PTV ≥ 36 Gy (5-fraction equivalent doses). All acute toxicities from SBRT were grade 1–2, and no myelopathy was observed.

CONCLUSIONS

Neoadjuvant high-dose, hypofractionated SBRT for spinal chordoma is safe and does not increase surgical morbidities. Early outcomes at 2 years are promising, although long-term follow-up is pending.

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Chengcheng Gui, Xuguang Chen, Khadija Sheikh, Liza Mathews, Sheng-Fu L. Lo, Junghoon Lee, Majid A. Khan, Daniel M. Sciubba, and Kristin J. Redmond

OBJECTIVE

In the treatment of spinal metastases with stereotactic body radiation therapy (SBRT), vertebral compression fracture (VCF) is a common and potentially morbid complication. Better methods to identify patients at high risk of radiation-induced VCF are needed to evaluate prophylactic measures. Radiomic features from pretreatment imaging may be employed to more accurately predict VCF. The objective of this study was to develop and evaluate a machine learning model based on clinical characteristics and radiomic features from pretreatment imaging to predict the risk of VCF after SBRT for spinal metastases.

METHODS

Vertebral levels C2 through L5 containing metastases treated with SBRT were included if they were naive to prior surgery or radiation therapy, target delineation was based on consensus guidelines, and 1-year follow-up data were available. Clinical features, including characteristics of the patient, disease, and treatment, were obtained from chart review. Radiomic features were extracted from the planning target volume (PTV) on pretreatment CT and T1-weighted MRI. Clinical and radiomic features selected by least absolute shrinkage and selection operator (LASSO) regression were included in random forest classification models, which were trained to predict VCF within 1 year after SBRT. Model performance was assessed with leave-one-out cross-validation.

RESULTS

Within 1 year after SBRT, 15 of 95 vertebral levels included in the analysis demonstrated new or progressive VCF. Selected clinical features included BMI, performance status, total prescription dose, dose to 99% of the PTV, lumbar location, and 2 components of the Spine Instability Neoplastic Score (SINS): lytic tumor character and spinal misalignment. Selected radiomic features included 5 features from CT and 3 features from MRI. The best-performing classification model, derived from a combination of selected clinical and radiomic features, demonstrated a sensitivity of 0.844, specificity of 0.800, and area under the receiver operating characteristic (ROC) curve (AUC) of 0.878. This model was significantly more accurate than alternative models derived from only selected clinical features (AUC = 0.795, p = 0.048) or only components of the SINS (AUC = 0.579, p < 0.0001).

CONCLUSIONS

In the treatment of spinal metastases with SBRT, a machine learning model incorporating both clinical features and radiomic features from pretreatment imaging predicted VCF at 1 year after SBRT with excellent sensitivity and specificity, outperforming models developed from clinical features or components of the SINS alone. If validated, these findings may allow more judicious selection of patients for prophylactic interventions.

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Ann Liu, Yike Jin, Ethan Cottrill, Majid Khan, Erick Westbroek, Jeff Ehresman, Zach Pennington, Sheng-fu L. Lo, Daniel M. Sciubba, Camilo A. Molina, and Timothy F. Witham

OBJECTIVE

Augmented reality (AR) is a novel technology which, when applied to spine surgery, offers the potential for efficient, safe, and accurate placement of spinal instrumentation. The authors report the accuracy of the first 205 pedicle screws consecutively placed at their institution by using AR assistance with a unique head-mounted display (HMD) navigation system.

METHODS

A retrospective review was performed of the first 28 consecutive patients who underwent AR-assisted pedicle screw placement in the thoracic, lumbar, and/or sacral spine at the authors’ institution. Clinical accuracy for each pedicle screw was graded using the Gertzbein-Robbins scale by an independent neuroradiologist working in a blinded fashion.

RESULTS

Twenty-eight consecutive patients underwent thoracic, lumbar, or sacral pedicle screw placement with AR assistance. The median age at the time of surgery was 62.5 (IQR 13.8) years and the median body mass index was 31 (IQR 8.6) kg/m2. Indications for surgery included degenerative disease (n = 12, 43%); deformity correction (n = 12, 43%); tumor (n = 3, 11%); and trauma (n = 1, 4%). The majority of patients (n = 26, 93%) presented with low-back pain, 19 (68%) patients presented with radicular leg pain, and 10 (36%) patients had documented lower extremity weakness. A total of 205 screws were consecutively placed, with 112 (55%) placed in the lumbar spine, 67 (33%) in the thoracic spine, and 26 (13%) at S1. Screw placement accuracy was 98.5% for thoracic screws, 97.8% for lumbar/S1 screws, and 98.0% overall.

CONCLUSIONS

AR depicted through a unique HMD is a novel and clinically accurate technology for the navigated insertion of pedicle screws. The authors describe the first 205 AR-assisted thoracic, lumbar, and sacral pedicle screws consecutively placed at their institution with an accuracy of 98.0% as determined by a Gertzbein-Robbins grade of A or B.

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Wataru Ishida, Joshua Casaos, Arun Chandra, Adam D’Sa, Seba Ramhmdani, Alexander Perdomo-Pantoja, Nicholas Theodore, George Jallo, Ziya L. Gokaslan, Jean-Paul Wolinsky, Daniel M. Sciubba, Ali Bydon, Timothy F. Witham, and Sheng-Fu L. Lo

OBJECTIVE

With the advent of intraoperative electrophysiological neuromonitoring (IONM), surgical outcomes of various neurosurgical pathologies, such as brain tumors and spinal deformities, have improved. However, its diagnostic and therapeutic value in resecting intradural extramedullary (ID-EM) spinal tumors has not been well documented in the literature. The objective of this study was to summarize the clinical results of IONM in patients with ID-EM spinal tumors.

METHODS

A retrospective patient database review identified 103 patients with ID-EM spinal tumors who underwent tumor resection with IONM (motor evoked potentials, somatosensory evoked potentials, and free-running electromyography) from January 2010 to December 2015. Patients were classified as those without any new neurological deficits at the 6-month follow-up (group A; n = 86) and those with new deficits (group B; n = 17). Baseline characteristics, clinical outcomes, and IONM findings were collected and statistically analyzed. In addition, a meta-analysis in compliance with the PRISMA guidelines was performed to estimate the overall pooled diagnostic accuracy of IONM in ID-EM spinal tumor resection.

RESULTS

No intergroup differences were discovered between the groups regarding baseline characteristics and operative data. In multivariate analysis, significant IONM changes (p < 0.001) and tumor location (thoracic vs others, p = 0.018) were associated with new neurological deficits at the 6-month follow-up. In predicting these changes, IONM yielded a sensitivity of 82.4% (14/17), specificity of 90.7% (78/86), positive predictive value (PPV) of 63.6% (14/22), negative predictive value (NPV) of 96.3% (78/81), and area under the curve (AUC) of 0.893. The diagnostic value slightly decreased in patients with schwannomas (AUC = 0.875) and thoracic tumors (AUC = 0.842). Among 81 patients who did not demonstrate significant IONM changes at the end of surgery, 19 patients (23.5%) exhibited temporary intraoperative exacerbation of IONM signals, which were recovered by interruption of surgical maneuvers; none of these patients developed new neurological deficits postoperatively. Including the present study, 5 articles encompassing 323 patients were eligible for this meta-analysis, and the overall pooled diagnostic value of IONM was a sensitivity of 77.9%, a specificity of 91.1%, PPV of 56.7%, and NPV of 95.7%.

CONCLUSIONS

IONM for the resection of ID-EM spinal tumors is a reasonable modality to predict new postoperative neurological deficits at the 6-month follow-up. Future prospective studies are warranted to further elucidate its diagnostic and therapeutic utility.

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Wuyang Yang, Jordina Rincon-Torroella, James Feghali, Adham M. Khalafallah, Wataru Ishida, Alexander Perdomo-Pantoja, Alfredo Quiñones-Hinojosa, Michael Lim, Gary L. Gallia, Gregory J. Riggins, William S. Anderson, Sheng-Fu Larry Lo, Daniele Rigamonti, Rafael J. Tamargo, Timothy F. Witham, Ali Bydon, Alan R. Cohen, George I. Jallo, Alban Latremoliere, Mark G. Luciano, Debraj Mukherjee, Alessandro Olivi, Lintao Qu, Ziya L. Gokaslan, Daniel M. Sciubba, Betty Tyler, Henry Brem, and Judy Huang

OBJECTIVE

International research fellows have been historically involved in academic neurosurgery in the United States (US). To date, the contribution of international research fellows has been underreported. Herein, the authors aimed to quantify the academic output of international research fellows in the Department of Neurosurgery at The Johns Hopkins University School of Medicine.

METHODS

Research fellows with Doctor of Medicine (MD), Doctor of Philosophy (PhD), or MD/PhD degrees from a non-US institution who worked in the Hopkins Department of Neurosurgery for at least 6 months over the past decade (2010–2020) were included in this study. Publications produced during fellowship, number of citations, and journal impact factors (IFs) were analyzed using ANOVA. A survey was sent to collect information on personal background, demographics, and academic activities.

RESULTS

Sixty-four international research fellows were included, with 42 (65.6%) having MD degrees, 17 (26.6%) having PhD degrees, and 5 (7.8%) having MD/PhD degrees. During an average 27.9 months of fellowship, 460 publications were produced in 136 unique journals, with 8628 citations and a cumulative journal IF of 1665.73. There was no significant difference in total number of publications, first-author publications, and total citations per person among the different degree holders. Persons holding MD/PhDs had a higher number of citations per publication per person (p = 0.027), whereas those with MDs had higher total IFs per person (p = 0.048). Among the 43 (67.2%) survey responders, 34 (79.1%) had nonimmigrant visas at the start of the fellowship, 16 (37.2%) were self-paid or funded by their country of origin, and 35 (81.4%) had mentored at least one US medical student, nonmedical graduate student, or undergraduate student.

CONCLUSIONS

International research fellows at the authors’ institution have contributed significantly to academic neurosurgery. Although they have faced major challenges like maintaining nonimmigrant visas, negotiating cultural/language differences, and managing self-sustainability, their scientific productivity has been substantial. Additionally, the majority of fellows have provided reciprocal mentorship to US students.

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Oluwaseun O. Akinduro, Diogo P. Garcia, Dominique M. O. Higgins, Tito Vivas-Buitrago, Mark Jentoft, David A. Solomon, David J. Daniels, Zach Pennington, Wendy J. Sherman, Mychael Delgardo, Mohamad Bydon, Maziyar A. Kalani, George Zanazzi, Nadejda Tsankova, Bernard R. Bendok, Paul C. McCormick, Daniel M. Sciubba, Sheng-fu Larry Lo, Jennifer L. Clarke, Kingsley Abode-Iyamah, and Alfredo Quiñones-Hinojosa

OBJECTIVE

High-grade spinal glioma (HGSG) is a rare but aggressive tumor that occurs in both adults and children. Histone H3 K27M mutation correlates with poor prognosis in children with diffuse midline glioma. However, the role of H3 K27M mutation in the prognosis of adults with HGSG remains unclear owing to the rarity of this mutation, conflicting reports, and the absence of multicenter studies on this topic.

METHODS

The authors studied a cohort of 30 adult patients with diffuse HGSG who underwent histological confirmation of diagnosis, surgical intervention, and treatment between January 2000 and July 2020 at six tertiary academic centers. The primary outcome was the effect of H3 K27M mutation status on progression-free survival (PFS) and overall survival (OS).

RESULTS

Thirty patients (18 males and 12 females) with a median (range) age of 50.5 (19–76) years were included in the analysis. Eighteen patients had H3 K27M mutation–positive tumors, and 12 had H3 K27M mutation–negative tumors. The median (interquartile range) PFS was 3 (10) months, and the median (interquartile range) OS was 9 (23) months. The factors associated with increased survival were treatment with concurrent chemotherapy/radiation (p = 0.006 for PFS, and p ≤ 0.001 for OS) and American Spinal Injury Association grade C or better at presentation (p = 0.043 for PFS, and p < 0.001 for OS). There were no significant differences in outcomes based on tumor location, extent of resection, sex, or H3 K27M mutation status. Analysis restricted to HGSG containing necrosis and/or microvascular proliferation (WHO grade IV histological features) revealed increased OS for patients with H3 K27M mutation–positive tumors (p = 0.017).

CONCLUSIONS

Although H3 K27M mutant–positive HGSG was associated with poor outcomes in adult patients, the outcomes of patients with H3 K27M mutant–positive HGSG were somewhat more favorable compared with those of their H3 K27M mutant–negative HGSG counterparts. Further preclinical animal studies and larger clinical studies are needed to further understand the age-dependent effects of H3 K27M mutation.

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Varun Puvanesarajah, Sheng-fu Larry Lo, Nafi Aygun, Jason A. Liauw, Ignacio Jusué-Torres, Ioan A. Lina, Uri Hadelsberg, Benjamin D. Elder, Ali Bydon, Chetan Bettegowda, Daniel M. Sciubba, Jean-Paul Wolinsky, Daniele Rigamonti, Lawrence R. Kleinberg, Ziya L. Gokaslan, Timothy F. Witham, Kristin J. Redmond, and Michael Lim

OBJECT

The number of patients with spinal tumors is rapidly increasing; spinal metastases develop in more than 30% of cancer patients during the course of their illness. Such lesions can significantly decrease quality of life, often necessitating treatment. Stereotactic radiosurgery has effectively achieved local control and symptomatic relief for these patients. The authors determined prognostic factors that predicted pain palliation and report overall institutional outcomes after spine stereotactic body radiation therapy (SBRT).

METHODS

Records of patients who had undergone treatment with SBRT for either primary spinal tumors or spinal metastases from June 2008 through June 2013 were retrospectively reviewed. Data were collected at the initial visit just before treatment and at 1-, 3-, 6-, and 12-month follow-up visits. Collected clinical data included Karnofsky Performance Scale scores, pain status, presence of neurological deficits, and prior radiation exposure at the level of interest. Radiation treatment plan parameters (dose, fractionation, and target coverage) were recorded. To determine the initial extent of epidural spinal cord compression (ESCC), the authors retrospectively reviewed MR images, assessed spinal instability according to the Bilsky scale, and evaluated lesion progression after treatment.

RESULTS

The study included 99 patients (mean age 60.4 years). The median survival time was 9.1 months (95% CI 6.9–17.2 months). Significant decreases in the proportion of patients reporting pain were observed at 3 months (p < 0.0001), 6 months (p = 0.0002), and 12 months (p = 0.0019) after treatment. Significant decreases in the number of patients reporting pain were also observed at the last follow-up visit (p = 0.00020) (median follow-up time 6.1 months, range 1.0–56.6 months). Univariate analyses revealed that significant predictors of persistent pain after intervention were initial ESCC grade, stratified by a Bilsky grade of 1c (p = 0.0058); initial American Spinal Injury Association grade of D (p = 0.011); initial Karnofsky Performance Scale score, stratified by a score of 80 (p = 0.002); the presence of multiple treated lesions (p = 0.044); and prior radiation at the site of interest (p < 0.0001). However, when multivariate analyses were performed on all variables with p values less than 0.05, the only predictor of pain at last follow-up visit was a prior history of radiation at the site of interest (p = 0.0038), although initial ESCC grade trended toward significance (p = 0.073). Using pain outcomes at 3 months, at this follow-up time point, pain could be predicted by receipt of radiation above a threshold biologically effective dose of 66.7 Gy.

CONCLUSIONS

Pain palliation occurs as early as 3 months after treatment; significant differences in pain reporting are also observed at 6 and 12 months. Pain palliation is limited for patients with spinal tumors with epidural extension that deforms the cord and for patients who have previously received radiation to the same site. Further investigation into the optimal dose and fractionation schedule are needed, but improved outcomes were observed in patients who received radiation at a biologically effective dose (with an a/b of 3.0) of 66.7 Gy or higher.