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Comparative study of on-label versus off-label treatment of intracranial aneurysms with the Pipeline embolization device

Samuel J. Cler, David C. Lauzier, Arindam R. Chatterjee, Joshua W. Osbun, Christopher J. Moran, and Akash P. Kansagra

OBJECTIVE

The Pipeline embolization device (PED) is widely used for the treatment of intracranial aneurysms, including in off-label applications. In this work, the authors compared the real-world efficacy and safety of PED use in on-label and off-label aneurysm treatments.

METHODS

Clinical and angiographic data of patients who underwent PED placement at a high-volume academic medical center were retrospectively obtained. Treatments were classified as on-label if they fell within the applications approved by the United States Food and Drug Administration as of 2021. Recorded outcomes included aneurysm occlusion, procedural complications, ischemic events, in-stent stenosis, intracranial hemorrhage, postprocedural functional status, and death.

RESULTS

In total, 416 aneurysms in 330 patients were treated with PED, comprising 256 aneurysms that received on-label treatments and 160 that received off-label treatments. The overall rate of complete aneurysm occlusion was 76.4% for on-label aneurysms and 75.6% for off-label aneurysms (p = 0.898). The risk of ischemic stroke in patients who underwent off-label treatments was 15.2%, which was higher than the 4.2% rate in patients who underwent on-label treatment (p = 0.003). All other clinical complications, procedural complications, and long-term functional status were comparable between the on-label and off-label groups.

CONCLUSIONS

In real-world practice, off-label use of PED is common and can achieve similar efficacy as on-label use. However, in aggregate, off-label use was found to carry an increased rate of ischemic complications. With judicious attention to safety and individual patient characteristics, these results highlight the scale and general feasibility of off-label PED use by experts.

In Journal of Neurosurgery Publish Before Print

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Decline of verbal fluency with lateral superior frontal gyrus penetration in subthalamic nucleus deep brain stimulation for Parkinson disease

Asra Askari, Taylor R. Greif, Jordan Lam, Amanda C. Maher, Carol C. Persad, and Parag G. Patil

OBJECTIVE

Verbal fluency (VF) decline is a well-recognized adverse cognitive outcome following subthalamic nucleus deep brain stimulation (STN DBS) in patients with Parkinson disease (PD). The mechanisms underlying VF decline, whether from stimulation, lesioning, or both, remain unclear. This study aims to investigate the unique effects of DBS lead trajectory on VF beyond previously reported effects of active contact location.

METHODS

The study population included 56 patients with idiopathic PD who underwent bilateral STN DBS. Phonemic and semantic VF scores were compared pre- and postoperatively. Features of the electrode trajectory were measured on postoperative imaging, including distance from the falx cerebri, distance from the superior frontal sulcus, and caudate nucleus penetration. The authors used t-tests, Pearson’s correlation, and multiple linear regression analyses to examine the relationship between VF change and demographic, disease, and electrode trajectory variables.

RESULTS

The laterality of entry within the left superior frontal gyrus (SFG) predicted greater phonemic VF decline (sr2 = 0.28, p < 0.001) after controlling for active contact location. VF change did not differ by the presence of caudate nucleus penetration in either hemisphere (p > 0.05).

CONCLUSIONS

Lateral penetration of the SFG in the left hemisphere is associated with worsening phonemic VF and has greater explanatory power than active contact location. This may be explained by lesioning of the lateral SFG–Broca area pathway, which is implicated in language function.

In Journal of Neurosurgery Publish Before Print

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Development of an integrated risk scale for prediction of shunt placement after neonatal intraventricular hemorrhage

Michael C. Jin, Jonathon J. Parker, Adrian J. Rodrigues, Gabriela D. Ruiz Colón, Cesar A. Garcia, Kelly B. Mahaney, Gerald A. Grant, and Laura M. Prolo

OBJECTIVE

Neonatal intraventricular hemorrhage (IVH) is a major cause of mortality and morbidity, particularly following premature birth. Even after the acute phase, posthemorrhagic hydrocephalus is a long-term complication, frequently requiring permanent ventriculoperitoneal shunt (VPS) placement. Currently, there are no risk classification methods integrating the constellation of clinical data to predict short- and long-term prognosis in neonatal IVH. To address this need, the authors developed a two-part machine learning approach for predicting short- and long-term outcomes after diagnosis of neonatal IVH. Integrating both maternal and neonatal characteristics, they developed a binary classifier to predict short-term mortality risk and a clinical scale to predict the long-term risk of VPS placement.

METHODS

Neonates with IVH were identified from the Optum Clinformatics Data Mart administrative claims database. Matched maternal and childbirth characteristics were obtained for all patients. The primary endpoints of interest were short-term (30 day) mortality and long-term VPS placement. Classification of short-term mortality risk was evaluated using 5 different machine learning approaches and the best-performing method was validated using a withheld validation subset. Prediction of long-term shunt risk was performed using a multivariable Cox regression model with stepwise variable selection, which was subsequently converted to an easily applied integer risk scale.

RESULTS

A total of 5926 neonates with IVH were identified. Most patients were born before 32 weeks’ gestation (67.2%) and with low birth weight (81.2%). Empirical 30-day mortality risk was 10.9% across all IVH grades and highest among grade IV IVH (34.3%). Among the neonates who survived > 30 days, actuarial 12-month postdiagnosis risk of shunt placement was 5.4% across all IVH grades and 31.3% for grade IV IVH. The optimal short-term risk classifier was a random forest model achieving an area under the receiver operating characteristic curve of 0.882 with important predictors ranging from gestational age to diverse comorbid medical conditions. Selected features for long-term shunt risk stratification were IVH grade, respiratory distress syndrome, disseminated intravascular coagulation, and maternal preeclampsia or eclampsia. An integer risk scale, termed the Shunt Prediction After IVH in Neonates (SPAIN) scale, was developed from these 4 features, which, evaluated on withheld cases, demonstrated improved risk stratification compared with IVH grade alone (Harrell’s concordance index 0.869 vs 0.852).

CONCLUSIONS

In a large cohort of neonates with IVH, the authors developed a two-pronged, integrated, risk classification approach to anticipate short-term mortality and long-term shunt risk. The application of such approaches may improve the prognostication of outcomes and identification of higher-risk individuals who warrant careful surveillance and early intervention.

In Journal of Neurosurgery: Pediatrics Publish Before Print

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Identifying risk factors for postoperative diabetes insipidus in more than 2500 patients undergoing transsphenoidal surgery: a single-institution experience

Rushikesh S. Joshi, Matheus P. Pereira, Robert C. Osorio, Taemin Oh, Alexander F. Haddad, Kaitlyn M. Pereira, Kevin C. Donohue, Zain Peeran, Sweta Sudhir, Saket Jain, Angad Beniwal, Ankush Chandra, Seunggu J. Han, John D. Rolston, Philip V. Theodosopoulos, Sandeep Kunwar, Lewis S. Blevins Jr., and Manish K. Aghi

OBJECTIVE

Diabetes insipidus (DI) following transsphenoidal surgery can adversely impact quality of life and be difficult to manage. This study sought to characterize pre- and perioperative risk factors that may predispose patients to DI after pituitary surgery.

METHODS

A retrospective review of patients treated at a single institution from 2007 to 2019 was conducted. DI was defined as postoperative sodium > 145 mEq/L and urine output > 300 ml/hr and/or postoperative desmopressin (ddAVP) use. DI was further characterized as transient or permanent. Uni- and multivariate analyses were performed to determine variables associated with postoperative DI.

RESULTS

The authors identified 2529 patients who underwent transsphenoidal surgery at their institution. Overall, DI was observed in 270 (10.7%) of the 2529 patients, with 114 (4.5%) having permanent DI and 156 (6.2%) with transient symptoms. By pathology type, DI occurred in 31 (46.3%) of 67 craniopharyngiomas, 10 (14.3%) of 70 apoplexies, 46 (14.3%) of 322 Rathke’s cleft cysts, 77 (7.7%) of 1004 nonfunctioning pituitary adenomas (NFPAs), and 62 (7.6%) of 811 functioning pituitary adenomas (FPAs). Final lesion pathology significantly affected DI rates (p < 0.001). Multivariate analysis across pathologies showed that younger age (odds ratio [OR] 0.97, p < 0.001), intraoperative CSF encounter (OR 2.74, p < 0.001), craniopharyngioma diagnosis (OR 8.22, p = 0.007), and postoperative hyponatremia (OR 1.50, p = 0.049) increased the risk of DI. Because surgery for each pathology created specific risk factors for DI, the analysis was then limited to the 1815 pituitary adenomas (PAs) in the series, comprising 1004 NFPAs and 811 FPAs. For PAs, younger age (PA: OR 0.97, p < 0.001; NFPA: OR 0.97, p < 0.001; FPA: OR 0.97, p = 0.028) and intraoperative CSF encounter (PA: OR 2.99, p < 0.001; NFPA: OR 2.93, p < 0.001; FPA: OR 3.06, p < 0.001) increased DI rates in multivariate analysis. Among all PAs, patients with DI experienced peak sodium levels later than those without DI (postoperative day 11 vs 2). Increasing tumor diameter increased the risk of DI in FPAs (OR 1.52, p = 0.008), but not in NFPAs (p = 0.564).

CONCLUSIONS

In more than 2500 patients treated at a single institution, intraoperative CSF encounter, craniopharyngioma diagnosis, and young age all increased the risk of postoperative DI. Patients with postoperative hyponatremia exhibited higher rates of DI, suggesting possible bi- or triphasic patterns to DI. Greater vigilance should be maintained in patients meeting these criteria following transsphenoidal surgery to ensure early recognition and treatment of DI.

In Journal of Neurosurgery Publish Before Print

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Incidence of repeat procedures and healthcare utilization following surgery, radiosurgery, and percutaneous procedures in elderly patients with trigeminal neuralgia

Mayur Sharma, Tyler Ball, Dengzhi Wang, Beatrice Ugiliweneza, Abbas Rattani, Shiao Woo, Maxwell Boakye, Joseph S. Neimat, Brian Williams, and Norberto Andaluz

OBJECTIVE

Management of trigeminal neuralgia (TN) in elderly patients poses significant challenges. The impact of different treatment modalities (surgery, radiosurgery [RS], and percutaneous techniques [PTs]) on healthcare utilization is not well defined in the management of TN in elderly patients. The aim of this study was to compare the long-term healthcare utilization metrics of different interventions in the management of elderly patients with TN.

METHODS

The MarketScan database was queried using the International Classification of Diseases, Ninth Revision and Current Procedural Terminology, from 2000 to 2016. TN patients ≥ 65 years of age managed using surgery, RS, and PTs with at least 5 years of follow-up after the index procedure were included. Outcomes analyzed were hospital admissions, outpatient services, and medication refills.

RESULTS

Of 993 patients, 43% (n = 430) underwent RS, 44% (n = 432) had PTs, and only 13% (n = 131) underwent surgery for TN. Overall, the median age of patients was 74 years old, 64% were females, 90% had Medicare insurance, and 17% had an Elixhauser index ≥ 3. Patients in the surgery group were younger (median age 71 years) with a higher comorbidity index (≥ 3; 24%) compared with patients undergoing RS and PTs (13% and 17%, respectively). At 1, 2, and 5 years after the index procedure, 41%, 48%, and 57% of patients in the PT cohort underwent any repeat procedure compared with 11%, 18%, and 29% for the RS cohort, and 6%, 9%, and 11% for the surgical cohort, respectively. Also, patients in the PT cohort incurred 1.8, 1.9, and 2.0 times the combined payment at 1, 2, and 5 years, respectively, compared with the surgery cohort. Similarly, patients who underwent RS for TN incurred 1.4, 1.5, and 1.5 times the combined payment at 1, 2, and 5 years, respectively, compared with the surgery cohort. At 5 years after the index procedure, combined payments for the PT cohort were $79,753 (IQR $46,013, $144,064) compared with $61,016 (IQR $27,114, $117,097) for the RS cohort and $41,074 (IQR $25,392, $87,952) for the surgery cohort (p < 0.0001).

CONCLUSIONS

PTs followed by RS were the common procedures used in the majority of elderly patients with TN. However, surgery for TN resulted in durable control with the least need for reoperations up to 5 years after the index procedure, followed by RS and PTs. PTs for TN resulted in the highest utilization of healthcare resources and need for reoperations at all time points. These findings should be considered in clinical decision-making when selecting appropriate treatment modalities in elderly patients with TN.

In Journal of Neurosurgery Publish Before Print

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Intra-arterial injection of mesenchymal stem cells to accelerate neointima formation after endovascular stenting in a rabbit model

Kapilan Panchendrabose, Sandeep Muram, Brooke L. Belanger, Muneer Eesa, Mohammed A. Almekhlafi, Mayank Goyal, John H. Wong, Arindom Sen, Bijoy K. Menon, Bryan Har, and Alim P. Mitha

OBJECTIVE

Delayed neointima formation over a neurovascular stent is associated with thrombotic complications that can lead to stroke. The purpose of this study was to evaluate whether an intra-arterial injection of mesenchymal stem cells (MSCs) after stent placement leads to improved neointima and reduced thrombus formation over the device.

METHODS

Solitaire stents were placed into the aortas of rabbits that were divided into MSC and control groups. The MSC group received an intra-arterial injection of MSCs through the same microcatheter used for stent deployment. Optical coherence tomography (OCT) was used to evaluate and compare neointima and thrombus formation in a blinded fashion. Explanted specimens were also imaged with scanning electron microscopy (SEM) and evaluated by observers blinded to group allocation using an endothelialization scoring system.

RESULTS

The 3-day MSC group was similar to the 7-day controls in terms of stent strut coverage ratio and maximum neointimal thickness, but these values were significantly higher than the 3-day control group based on a hierarchical mixed-effects linear regression analysis. SEM revealed a significantly higher endothelialization score for the MSC group compared with controls at the same time point. There was no difference in thrombus formation between any of the groups.

CONCLUSIONS

The intra-arterial injection of MSCs after endovascular stenting accelerated early neointima formation but had no effect on thrombus formation in this study. Larger studies are required to verify these findings and determine the durability and mechanism of this effect.

In Journal of Neurosurgery Publish Before Print

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Motor speech effects in subthalamic deep brain stimulation for Parkinson’s disease

Karen J. Kluin, James M. Mossner, Joseph T. Costello, Kelvin L. Chou, and Parag G. Patil

OBJECTIVE

A motor speech disorder or dysarthria commonly arises in patients with Parkinson’s disease (PD). The impact of subthalamic nucleus (STN) deep brain stimulation (DBS) on motor speech and the potential of intraoperative motor speech testing to predict outcomes are unknown. This study examined 1) the types and prevalence of motor speech changes observed with STN DBS and their relation to the preoperative condition, 2) the ability of intraoperative testing to predict postoperative changes in motor speech, and 3) the spatial relationship between stimulation sites producing maximal motor improvement, as measured by the Movement Disorder Society Unified Parkinson’s Disease Rating Scale (MDS-UPDRS), and maximal motor speech deterioration.

METHODS

Comprehensive preoperative, intraoperative, and postoperative motor speech/dysarthria evaluations were performed in consecutive patients with advanced idiopathic PD who underwent STN DBS surgery in the period from 2011 to 2016. Preoperative type of dysarthria and overall dysarthria severity rating along with intraoperative motor speech testing results were evaluated as predictors of postoperative change. Atlas-independent, fully individualized field modeling was used to identify stimulation sites associated with maximal MDS-UPDRS motor improvement and motor speech deterioration.

RESULTS

Forty-three patients with PD treated with STN DBS were prospectively studied. Improved MDS-UPDRS motor scores and worsened dysarthria were demonstrated by a subset of patients (16/43). Preoperative dysarthria characteristics did not predict postoperative deterioration. Intraoperative assessment of motor speech strongly predicted postoperative outcomes (OR 4.4, p = 0.02). Sites of maximal MDS-UPDRS motor improvement and worsened dysarthria were distinct. Worsened dysarthria was associated with capsular stimulation, anterior and ventral to the site of maximal MDS-UPDRS motor improvement.

CONCLUSIONS

The predictive reliability of intraoperative motor speech testing, together with the identification of distinct stimulation sites for motor speech impairment and improved MDS-UPDRS motor function, raise the possibility that DBS lead repositioning or reprogramming could reduce adverse effects on motor speech without impacting MDS-UPDRS motor outcomes in patients undergoing STN DBS.

In Journal of Neurosurgery Publish Before Print

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Noninvasive electrical stimulation as an adjunct to fusion procedures: a systematic review and meta-analysis

Abhijith V. Matur, Zachary J. Plummer, Juan C. Mejia-Munne, Monir Tabbosha, Justin N. Virojanapa, Rani Nasser, and Joseph S. Cheng

OBJECTIVE

Noninvasive electrical stimulation represents a distinct group of devices used to augment fusion rates. However, data regarding outcomes of noninvasive electrical stimulation have come from a small number of studies. The goal of this systematic review and meta-analysis was to determine outcomes of noninvasive electrical stimulation used as an adjunct to fusion procedures to improve rates of successful fusion.

METHODS

PubMed, Embase, and the Cochrane Clinical Trials database were searched according to search strategy and PRISMA guidelines. Random-effects meta-analyses of fusion rates with the three main modalities of noninvasive electrical stimulation, capacitively coupled stimulation (CCS), pulsed electromagnetic fields (PEMFs), and combined magnetic fields (CMFs), were conducted using R version 4.1.0 (The R Foundation for Statistical Computing). Both retrospective studies and clinical trials were included. Animal studies were excluded. Risk-of-bias analysis was performed with the Risk of Bias 2 (RoB 2) and Risk of Bias in Nonrandomized Studies of Interventions (ROBINS-I) tools.

RESULTS

Searches of PubMed, Embase, and the Cochrane Clinical Trials database identified 8 articles with 1216 participants meeting criteria from 213 initial results. There was a high overall risk of bias identified for the majority of randomized studies. No meta-analysis could be performed for CCS as only 1 study was identified. Meta-analysis of 6 studies of fusion rates in PEMF did not find any difference between treatment and control groups (OR 1.89, 95% CI 0.36–9.80, p = 0.449). Meta-analysis of 2 studies of CMF found no difference in fusion rates between control and treatment groups (OR 0.90, 95% CI 0.07–11.93, p = 0.939). Subgroup analysis of PEMF was limited given the small number of studies and patients, although significantly increased fusion rates were seen in some subgroups.

CONCLUSIONS

This meta-analysis of clinical outcomes and fusion rates in noninvasive electrical stimulation compared to no stimulation did not identify any increases in fusion rates for any modality. A high degree of heterogeneity between studies was noted. Although subgroup analysis identified significant differences in fusion rates in certain groups, these findings were based on a small number of studies and further research is needed. This analysis does not support routine use of these devices to augment fusion rates, although the data are limited by a high risk of bias and a small number of available studies.

In Journal of Neurosurgery: Spine Publish Before Print

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Parietal bone thickness for predicting operative transfusion and blood loss in patients undergoing spring-mediated cranioplasty for nonsyndromic sagittal craniosynostosis

Dillan F. Villavisanis, Daniel Y. Cho, Sameer Shakir, Christopher L. Kalmar, Connor S. Wagner, Liana Cheung, Jessica D. Blum, Shih-Shan Lang, Gregory G. Heuer, Peter J. Madsen, Scott P. Bartlett, Jordan W. Swanson, Jesse A. Taylor, and Alexander M. Tucker

OBJECTIVE

Variables that can predict outcomes in patients with craniosynostosis, including bone thickness, are important for surgical decision-making, yet are incompletely understood. Recent studies have demonstrated relative risks and benefits of surgical techniques for correcting head shape in patients with nonsyndromic sagittal craniosynostosis. The purpose of this study was to characterize the relationships between parietal bone thickness and perioperative outcomes in patients who underwent spring-mediated cranioplasty (SMC) for nonsyndromic sagittal craniosynostosis.

METHODS

Patients who underwent craniectomy and SMC for nonsyndromic sagittal craniosynostosis at a quaternary pediatric hospital between 2011 and 2021 were included. Parietal bone thickness was determined on patient preoperative CT at 27 suture-related points: at the suture line and at 0.5 cm, 1.0 cm, 1.5 cm, and 2.0 cm from the suture at the anterior parietal, midparietal, and posterior parietal bones. Preoperative skull thickness was compared with intraoperative blood loss, need for intraoperative transfusion, and hospital length of stay (LOS).

RESULTS

Overall, 124 patients with a mean age at surgery ± SD of 3.59 ± 0.87 months and mean parietal bone thickness of 1.83 ± 0.38 mm were included in this study. Estimated blood loss (EBL) and EBL per kilogram were associated with parietal bone thickness 0.5 cm (ρ = 0.376, p < 0.001 and ρ = 0.331, p = 0.004; respectively) and 1.0 cm (ρ = 0.324, p = 0.007 and ρ = 0.245, p = 0.033; respectively) from the suture line. Patients with a thicker parietal bone 0.5 cm (OR 18.08, p = 0.007), 1.0 cm (OR 7.16, p = 0.031), and 1.5 cm (OR 7.24, p = 0.046) from the suture line were significantly more likely to have undergone transfusion when controlling for age, sex, and race. Additionally, parietal bone thickness was associated with hospital LOS (β 0.575, p = 0.019) when controlling for age, sex, and race. Patient age at the time of surgery was not independently associated with these perioperative outcomes.

CONCLUSIONS

Parietal bone thickness, but not age at the time of surgery, may predict perioperative outcomes including transfusion, EBL, and LOS. The need for transfusion and EBL were most significant for parietal bone thickness 0.5 cm to 1.5 cm from the suture line, within the anticipated area of suturectomy. For patients undergoing craniofacial surgery, parietal bone thickness may have important implications for anticipating the need for intraoperative transfusion and hospital LOS.

In Journal of Neurosurgery: Pediatrics Publish Before Print

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Recrudescent infection after deep brain stimulator reimplantation

Matthew Moser, Shripadh Chitta, Patrick F. O’Brien, Andrew Caras, and Kathryn L. Holloway

OBJECTIVE

The efficacy of deep brain stimulation (DBS) in treating the symptoms of movement disorders can be life changing for patients. Thus, the 5%–15% incidence of stimulator-related infection requiring removal of the device can be particularly disheartening. Although DBS system reimplantation is generally successful, this is not always the case. The literature is replete with publications describing the incidence of infection and the associated features. However, the literature is sparse in terms of information on the incidence of recurrent or recrudescent infection after system reimplantation. The goal of this paper was to evaluate factors leading to unsuccessful reimplantation of a DBS system following initial infection.

METHODS

Data were reviewed for all DBS procedures performed by one surgeon (K.L.H.) over 19 years including the infectious agent, location of infection, treatment regimen, and subsequent reimplantation of a DBS system and long-term outcome.

RESULTS

In this series of 558 patients who had undergone DBS surgery, 37 (6.6%) subsequently developed an infection. Infections with methicillin-sensitive Staphylococcus aureus, Enterobacter species, or coagulase-negative staphylococci were predominant. Four patients had cerebritis, one had meningitis, and the rest had soft tissue infections of the pocket or scalp. All had their entire DBS system explanted, followed by 4–6 weeks of intravenous antibiotics and surveillance for recrudescence for an additional period of at least 30 days. Twenty-five patients subsequently underwent DBS system reimplantation, and the procedure was successful in 22. Three of the 4 patients with cerebritis developed a subsequent wound infection after system reimplantation. None of the other 22 patients developed a recurrence. The odds ratio for developing a recurrent infection after cerebritis was 28.5 (95% CI 1.931–420.5, p = 0.007).

CONCLUSIONS

This study, the largest series of DBS system reimplantations following infection, demonstrated that most patients can have successful reimplantations without recurrent infection. However, patients who have had DBS-related cerebritis have a nearly 30-fold increased risk of developing reinfection after reimplantation. Alternative strategies for these patients are discussed.

In Journal of Neurosurgery Publish Before Print