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Rebecca L. Achey, Erin Yamamoto, Daniel Sexton, Christine Hammer, Bryan S. Lee, Robert S. Butler, Nicolas R. Thompson, Sean J. Nagel, Andre G. Machado and Darlene A. Lobel

OBJECTIVE

Deep brain stimulation (DBS) is an effective therapy for movement disorders such as idiopathic Parkinson’s disease (PD) and essential tremor (ET). However, some patients who demonstrate benefit on objective motor function tests do not experience postoperative improvement in depression or anxiety, 2 important components of quality of life (QOL). Thus, to examine other possible explanations for the lack of a post-DBS correlation between improved objective motor function and decreased depression or anxiety, the authors investigated whether patient perceptions of motor symptom severity might contribute to disease-associated depression and anxiety.

METHODS

The authors performed a retrospective chart review of PD and ET patients who had undergone DBS at the Cleveland Clinic in the period from 2009 to 2013. Patient demographics, diagnosis (PD, ET), motor symptom severity, and QOL measures (Primary Care Evaluation of Mental Disorders 9-item Patient Health Questionnaire [PHQ-9] for depression, Generalized Anxiety Disorder 7-item Scale [GAD-7], and patient-assessed tremor scores) were collected at 4 time points: preoperatively, postoperatively, 1-year follow-up, and 2-year follow-up. Multivariable prediction models with solutions for fixed effects were constructed to assess the correlation of predictor variables with PHQ-9 and GAD-7 scores. Predictor variables included age, sex, visit time, diagnosis (PD vs ET), patient-assessed tremor, physician-reported tremor, Unified Parkinson’s Disease Rating Scale part III (UPDRS-III) score, and patient-assessed tremor over time.

RESULTS

Seventy PD patients and 17 ET patients were included in this analysis. Mean postoperative and 1-year follow-up UPDRS-III and physician-reported tremor scores were significantly decreased compared with preoperative scores (p < 0.0001). Two-year follow-up physician-reported tremor was also significantly decreased from preoperative scores (p < 0.0001). Only a diagnosis of PD (p = 0.0047) and the patient-assessed tremor rating (p < 0.0001) were significantly predictive of depression. A greater time since surgery, in general, significantly decreased anxiety scores (p < 0.0001) except when a worsening of patient-assessed tremor was reported over the same time period (p < 0.0013).

CONCLUSIONS

Patient-assessed tremor severity alone was predictive of depression in PD and ET following DBS. This finding suggests that a patient’s perception of illness plays a greater role in depression than objective physical disability regardless of the time since surgical intervention. In addition, while anxiety may be attenuated by DBS, patient-assessed return of tremor over time can increase anxiety, highlighting the importance of long-term follow-up for behavioral health features in chronic neurological disorders. Together, these data suggest that the patient experience of motor symptoms plays a role in depression and anxiety—a finding that warrants consideration when evaluating, treating, and following movement disorder patients who are candidates for DBS.

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Ayman El-Menyar, Mohammad Asim, Rifat Latifi, Shrikant I. Bangdiwala and Hassan Al-Thani

OBJECTIVE

The clinical relevance of high-sensitivity troponin T (HsTnT) in trauma patients is not well explored. In this study, the authors aimed to study the predictive value of serum HsTnT in intubated patients who had sustained traumatic brain injury (TBI).

METHODS

A retrospective analysis was conducted for all intubated TBI patients between 2010 and 2014 at a national level 1 trauma center. Data were analyzed and compared based on the HsTnT status on admission (group 1, negative results; and group 2, positive results). Receiver operating characteristic curves were used to determine sensitivity, specificity, and cutoff level of HsTnT to predict mortality. Time to earlier discharge from hospital or death was modeled using Cox proportional hazard models to describe the relationship between HsTnT and in-hospital mortality.

RESULTS

Of the 826 intubated TBI patients, 490 underwent HsTnT testing; 65.7% had positive HsTnT results. Patients in group 2 had a higher Injury Severity Score (p = 0.001) and head Abbreviated Injury Scale (AIS) score (p = 0.004) than those in group 1. In addition, group 2 patients were more likely to have lower Glasgow Coma Scale scores (p = 0.001) and more likely to experience intraventricular hemorrhage, brain edema, pneumonia, and sepsis (p = 0.001). HsTnT values positively correlated with head AIS score (r = 0.19, p = 0.001) and varied by the type of lesion and time to death. Ventilator days and length of hospital stay were more prolonged in group 2 patients (p = 0.001). Area under the curve (AUC) analysis showed that HsTnT ≥ 26.5 ng/L predicted all-cause mortality (AUC 0.75, 95% CI 0.699–0.801) with 80% sensitivity. Positive HsTnT was an independent predictor of mortality in multivariate models (adjusted OR 3.10, 95% CI 1.308–7.351) even after excluding chest injury (adjusted OR 4.18, 95% CI 1.320–13.231).

CONCLUSIONS

Positive HsTnT results are associated with poor outcomes in intubated patients with TBI. In this subset of patients, measuring serum HsTnT on admission is a useful tool for early risk stratification and expedited care; however, further prospective studies are warranted.

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Linda S. Aglio, Muhammad M. Abd-El-Barr, Vwaire Orhurhu, Grace Y. Kim, Jie Zhou, Laverne D. Gugino, Lisa J. Crossley, James L. Gosnell, John H. Chi and Michael W. Groff

OBJECTIVE

Preemptive administration of analgesic medication is more effective than medication given after the onset of the painful stimulus. The efficacy of preoperative or preemptive pain relief after thoracolumbosacral spine surgery has not been well studied. The present study was a double-blind, placebo-controlled randomized trial of preemptive analgesia with a single-shot epidural injection in adult patients undergoing spine surgery.

METHODS

Ninety-nine adult patients undergoing thoracolumbosacral operations via a posterior approach were randomized to receive a single shot of either epidural placebo (group 1), hydromorphone alone (group 2), or bupivacaine with hydromorphone (group 3) before surgery at the preoperative holding area. The primary outcome was the presence of opioid sparing and rescue time—defined as the time interval from when a patient was extubated to the time pain medication was first demanded during the postoperative period. Secondary outcomes include length of stay at the postanesthesia care unit (PACU), pain score at the PACU, opioid dose, and hospital length of stay.

RESULTS

Of the 99 patients, 32 were randomized to the epidural placebo group, 33 to the hydromorphone-alone group, and 34 to the bupivacaine with hydromorphone group. No significant difference was seen across the demographics and surgical complexities for all 3 groups. Compared to the control group, opioid sparing was significantly higher in group 2 (57.6% vs 15.6%, p = 0.0007) and group 3 (52.9% vs 15.6%, p = 0.0045) in the first demand of intravenous hydromorphone as a supplemental analgesic medication. Compared to placebo, the rescue time was significantly higher in group 2 (187 minutes vs 51.5 minutes, p = 0.0014) and group 3 (204.5 minutes vs 51. minutes, p = 0.0045). There were no significant differences in secondary outcomes.

CONCLUSIONS

The authors’ study demonstrated that preemptive analgesia in thoracolumbosacral surgeries can significantly reduce analgesia requirements in the immediate postoperative period as evidenced by reduced request for opioid medication in both analgesia study groups who received a preoperative analgesic epidural. Nonetheless, the lack of differences in pain score and opioid dose at the PACU brings into question the role of preemptive epidural opioids in spine surgery patients. Further work is necessary to investigate the long-term effectiveness of preemptive epidural opioids and their role in pain reduction and patient satisfaction.

Clinical trial registration no.: NCT02968862 (clinicaltrials.gov)

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Constantin Tuleasca, Jean Régis, Elena Najdenovska, Tatiana Witjas, Nadine Girard, Thomas Bolton, Francois Delaire, Marion Vincent, Mohamed Faouzi, Jean-Philippe Thiran, Meritxell Bach Cuadra, Marc Levivier and Dimitri Van de Ville

OBJECTIVE

Essential tremor (ET) is the most common movement disorder. Drug-resistant ET can benefit from standard stereotactic deep brain stimulation or radiofrequency thalamotomy or, alternatively, minimally invasive techniques, including stereotactic radiosurgery (SRS) and high-intensity focused ultrasound, at the level of the ventral intermediate nucleus (Vim). The aim of the present study was to evaluate potential correlations between pretherapeutic interconnectivity (IC), as depicted on resting-state functional MRI (rs-fMRI), and MR signature volume at 1 year after Vim SRS for tremor, to be able to potentially identify hypo- and hyperresponders based only on pretherapeutic neuroimaging data.

METHODS

Seventeen consecutive patients with ET were included, who benefitted from left unilateral SRS thalamotomy (SRS-T) between September 2014 and August 2015. Standard tremor assessment and rs-fMRI were acquired pretherapeutically and 1 year after SRS-T. A healthy control group was also included (n = 12). Group-level independent component analysis (ICA; only n = 17 for pretherapeutic rs-fMRI) was applied. The mean MR signature volume was 0.125 ml (median 0.063 ml, range 0.002–0.600 ml). The authors correlated baseline IC with 1-year MR signatures within all networks. A 2-sample t-test at the level of each component was first performed in two groups: group 1 (n = 8, volume < 0.063 ml) and group 2 (n = 9, volume ≥ 0.063 ml). These groups did not statistically differ by age, duration of symptoms, baseline ADL score, ADL point decrease at 1 year, time to tremor arrest, or baseline tremor score on the treated hand (TSTH; p > 0.05). An ANOVA was then performed on each component, using individual subject-level maps and continuous values of 1-year MR signatures, correlated with pretherapeutic IC.

RESULTS

Using 2-sample t-tests, two networks were found to be statistically significant: network 3, including the brainstem, motor cerebellum, bilateral thalamus, and left supplementary motor area (SMA) (pFWE = 0.004, cluster size = 94), interconnected with the red nucleus (MNI −2, −22, −32); and network 9, including the brainstem, posterior insula, bilateral thalamus, and left SMA (pFWE = 0.002, cluster size = 106), interconnected with the left SMA (MNI 24, −28, 44). Higher pretherapeutic IC was associated with higher MR volumes, in a network including the anterior default-mode network and bilateral thalamus (ANOVA, pFWE = 0.004, cluster size = 73), interconnected with cerebellar lobule V (MNI −12, −70, −22). Moreover, in the same network, radiological hyporesponders presented with negative IC values.

CONCLUSIONS

These findings have clinical implications for predicting MR signature volumes after SRS-T. Here, using pretherapeutic MRI and data processing without prior hypothesis, the authors showed that pretherapeutic network interconnectivity strength predicts 1-year MR signature volumes following SRS-T.

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Herwin Speckter, Jose Bido, Giancarlo Hernandez, Diones Rivera, Luis Suazo, Santiago Valenzuela, Isidro Miches, Jairo Oviedo, Cesar Gonzalez and Peter Stoeter

OBJECTIVE

The goal of this study was to identify parameters from routine T1- and T2-weighted MR sequences and diffusion tensor imaging (DTI) that best predict the volumetric changes in a meningioma after treatment with Gamma Knife radiosurgery (GKRS).

METHODS

In 32 patients with meningioma, routine MRI and DTI data were measured before GKRS. A total of 78 parameters derived from first-level texture analysis of the pretreatment MR images, including calculation of the mean, SD, 2.5th and 97.5th percentiles, and kurtosis and skewness of data in histograms on a voxel-wise basis, were correlated with lesion volume change after a mean follow-up period of 3 years (range 19.5–63.3 months).

RESULTS

Several DTI-derived parameters correlated significantly with a meningioma volume change. The parameter that best predicted the results of GKRS was the 2.5th percentile value of the smallest eigenvalue (L3) of the diffusion tensor (correlation coefficient 0.739, p ≤ 0.001), whereas among the non-DTI parameters, only the SD of T2-weighted images correlated significantly with a tumor volume change (correlation coefficient 0.505, p ≤ 0.05, after correction for family-wise errors using false-detection-rate correction).

CONCLUSIONS

DTI-derived data had a higher correlation to shrinkage of meningioma volume after GKRS than data from T1- and T2-weighted image sequences. However, if only routine MR images are available, the SD of T2-weighted images can be used to predict control or possible progression of a meningioma after GKRS.

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Veronica L. Chiang, Samuel T. Chao, Constantin Tuleasca, Matthew C. Foote, Cheng-chia Lee, David Mathieu, Hany Soliman and Arjun Sahgal

In order to determine what areas of research are a clinical priority, a small group of young Gamma Knife investigators was invited to attend a workshop discussion at the 19th International Leksell Gamma Knife Society Meeting. Two areas of interest and the need for future radiosurgical research involving multiple institutions were identified by the young investigators working group: 1) the development of additional imaging sequences to guide the understanding, treatment, and outcome tracking of diseases such as tremor, radiation necrosis, and AVM; and 2) trials to clarify the role of hypofractionation versus single-fraction radiosurgery in the treatment of large lesions such as brain metastases, postoperative cavities, and meningiomas.

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Masaaki Yamamoto, Toru Serizawa, Yoshinori Higuchi, Osamu Nagano, Hitoshi Aiyama, Takao Koiso, Shinya Watanabe, Takuya Kawabe, Yasunori Sato and Hidetoshi Kasuya

OBJECTIVE

With the aging of the population, increasing numbers of elderly patients with brain metastasis (BM) are undergoing stereotactic radiosurgery (SRS). Among recently reported prognostic grading indexes, only the basic score for brain metastases (BSBM) is applicable to patients 65 years or older. However, the major weakness of this system is that no BM-related factors are graded. This prompted the authors to develop a new grading system, the elderly-specific (ES)–BSBM.

METHODS

For this IRB-approved, retrospective cohort study, the authors used their prospectively accumulated database comprising 3267 consecutive patients undergoing Gamma Knife SRS for BMs during the 1998–2016 period at the Mito GammaHouse. Among these 3267 patients, 1789 patients ≥ 65 years of age were studied (Yamamoto series [Y-series]). Another series of 1785 patients ≥ 65 years of age in whom Serizawa and colleagues performed Gamma Knife SRS during the same period (Serizawa series [S-series]) was used for validity testing of the ES-BSBM.

RESULTS

Two factors were identified as strongly impacting longer survival after SRS by means of multivariable analysis using the Cox proportional hazard model with a stepwise selection procedure. These factors are the number of tumors (solitary vs multiple: HR 1.450, 95% CI 1.299–1.621; p < 0.0001) and cumulative tumor volume (≤ 15 cm3 vs > 15 cm3: HR 1.311, 95% CI 1.078–1.593; p = 0.0067). The new index is the addition of scores 0 and 1 for these 2 factors to the BSBM. The ES-BSBM system is based on categorization into 3 classes by adding these 2 scores to those of the original BSBM. Each ES-BSBM category has 2 possible scores. For the category ES-BSBM 4–5, the score is either 4 or 5; for ES-BSBM 2–3, the score is either 2 or 3; and for ES-BSBM 0–1, the score is either 0 or 1. In the Y-series, the median survival times (MSTs, months) after SRS were 17.5 (95% CI 15.4–19.3) in ES-BSBM 4–5, 6.9 (95% CI 6.4–7.4) in ES-BSBM 2–3, and 2.8 (95% CI 2.5–3.6) in ES-BSBM 0–1 (p < 0.0001). Also, in the S-series, MSTs were, respectively, 20.4 (95% CI 17.2–23.4), 7.9 (95% CI 7.4–8.5), and 3.2 (95% CI 2.8–3.6) (p < 0.0001). The ES-BSBM system was shown to be applicable to patients with all primary tumor types as well as to those 80 years or older.

CONCLUSIONS

The authors found that the addition of the number of tumors and cumulative tumor volume as scoring factors to the BSBM system significantly improved the prognostic value of this index. The present study is strengthened by testing the ES-BSBM in a different patient group.

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Marc Levivier, Rafael E. Carrillo, Rémi Charrier, André Martin and Jean-Philippe Thiran

OBJECTIVE

The authors developed a new, real-time interactive inverse planning approach, based on a fully convex framework, to be used for Gamma Knife radiosurgery.

METHODS

The convex framework is based on the precomputation of a dictionary composed of the individual dose distributions of all possible shots, considering all their possible locations, sizes, and shapes inside the target volume. The convex problem is solved to determine the plan, i.e., which shots and with which weights, that will actually be used, considering a sparsity constraint on the shots to fulfill the constraints while minimizing the beam-on time. The system is called IntuitivePlan and allows data to be transferred from generated dose plans into the Gamma Knife treatment planning software for further dosimetry evaluation.

RESULTS

The system has been very efficiently implemented, and an optimal plan is usually obtained in less than 1 to 2 minutes, depending on the complexity of the problem, on a desktop computer or in only a few minutes on a high-end laptop. Dosimetry data from 5 cases, 2 meningiomas and 3 vestibular schwannomas, were generated with IntuitivePlan. Results of evaluation of the dosimetry characteristics are very satisfactory and adequate in terms of conformity, selectivity, gradient, protection of organs at risk, and treatment time.

CONCLUSIONS

The possibility of using optimal, interactive real-time inverse planning in conjunction with the Leksell Gamma Knife opens new perspectives in radiosurgery, especially considering the potential use of the full capabilities of the latest generations of the Leksell Gamma Knife. This approach gives new users the possibility of using the system for easier and quicker access to good-quality plans with a shorter technical training period and opens avenues for new planning strategies for expert users. The use of a convex optimization approach allows an optimal plan to be provided in a very short processing time. This way, innovative graphical user interfaces can be developed, allowing the user to interact directly with the planning system to graphically define the desired dose map and to modify on-the-fly the dose map by moving, in a very user-friendly manner, the isodose surfaces of an initial plan. Further independent quantitative prospective evaluation comparing inverse planned and forward planned cases is warranted to validate this novel and promising treatment planning approach.

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Sameer Kitab, Bryan S. Lee and Edward C. Benzel

OBJECTIVE

Using an imaging-based prospective comparative study of 709 eligible patients that was designed to assess lumbar spinal stenosis (LSS) in the ages between 16 and 82 years, the authors aimed to determine whether they could formulate radiological structural differences between the developmental and degenerative types of LSS.

METHODS

MRI structural changes were prospectively reviewed from 2 age cohorts of patients: those who presented clinically before the age of 60 years and those who presented at 60 years or older. Categorical degeneration variables at L1–S1 segments were compared. A multivariate comparative analysis of global radiographic degenerative variables and spinal dimensions was conducted in both cohorts. The age at presentation was correlated as a covariable.

RESULTS

A multivariate analysis demonstrated no significant between-groups differences in spinal canal dimensions and stenosis grades in any segments after age was adjusted for. There were no significant variances between the 2 cohorts in global degenerative variables, except at the L4–5 and L5–S1 segments, but with only small effect sizes. Age-related degeneration was found in the upper lumbar segments (L1–4) more than the lower lumbar segments (L4–S1). These findings challenge the notion that stenosis at L4–5 and L5–S1 is mainly associated with degenerative LSS.

CONCLUSIONS

Integration of all the morphometric and qualitative characteristics of the 2 LSS cohorts provides evidence for a developmental background for LSS. Based on these findings the authors propose the concept of LSS as a developmental syndrome with superimposed degenerative changes. Further studies can be conducted to clarify the clinical definition of LSS and appropriate management approaches.

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Ethan A. Winkler, Harjus Birk, Jan-Karl Burkhardt, Xiaolin Chen, John K. Yue, Diana Guo, W. Caleb Rutledge, George F. Lasker, Carlene Partow, Tarik Tihan, Edward F. Chang, Hua Su, Helen Kim, Brian P. Walcott and Michael T. Lawton

OBJECTIVE

Brain arteriovenous malformations (bAVMs) are rupture-prone tangles of blood vessels with direct shunting of blood flow between arterial and venous circulations. The molecular and/or cellular mechanisms contributing to bAVM pathogenesis and/or destabilization in sporadic lesions have remained elusive. Initial insights into AVM formation have been gained through models of genetic AVM syndromes. And while many studies have focused on endothelial cells, the contributions of other vascular cell types have yet to be systematically studied. Pericytes are multifunctional mural cells that regulate brain angiogenesis, blood-brain barrier integrity, and vascular stability. Here, the authors analyze the abundance of brain pericytes and their association with vascular changes in sporadic human AVMs.

METHODS

Tissues from bAVMs and from temporal lobe specimens from patients with medically intractable epilepsy (nonvascular lesion controls [NVLCs]) were resected. Immunofluorescent staining with confocal microscopy was performed to quantify pericytes (platelet-derived growth factor receptor–beta [PDGFRβ] and aminopeptidase N [CD13]) and extravascular hemoglobin. Iron-positive hemosiderin deposits were quantified with Prussian blue staining. Syngo iFlow post–image processing was used to measure nidal blood flow on preintervention angiograms.

RESULTS

Quantitative immunofluorescent analysis demonstrated a 68% reduction in the vascular pericyte number in bAVMs compared with the number in NVLCs (p < 0.01). Additional analysis demonstrated 52% and 50% reductions in the vascular surface area covered by CD13- and PDGFRβ-positive pericyte cell processes, respectively, in bAVMs (p < 0.01). Reductions in pericyte coverage were statistically significantly greater in bAVMs with prior rupture (p < 0.05). Unruptured bAVMs had increased microhemorrhage, as evidenced by a 15.5-fold increase in extravascular hemoglobin compared with levels in NVLCs (p < 0.01). Within unruptured bAVM specimens, extravascular hemoglobin correlated negatively with pericyte coverage (CD13: r = −0.93, p < 0.01; PDGFRβ: r = −0.87, p < 0.01). A similar negative correlation was observed with pericyte coverage and Prussian blue–positive hemosiderin deposits (CD13: r = −0.90, p < 0.01; PDGFRβ: r = −0.86, p < 0.01). Pericyte coverage positively correlated with the mean transit time of blood flow or the time that circulating blood spends within the bAVM nidus (CD13: r = 0.60, p < 0.05; PDGFRβ: r = 0.63, p < 0.05). A greater reduction in pericyte coverage is therefore associated with a reduced mean transit time or faster rate of blood flow through the bAVM nidus. No correlations were observed with time to peak flow within feeding arteries or draining veins.

CONCLUSIONS

Brain pericyte number and coverage are reduced in sporadic bAVMs and are lowest in cases with prior rupture. In unruptured bAVMs, pericyte reductions correlate with the severity of microhemorrhage. A loss of pericytes also correlates with a faster rate of blood flow through the bAVM nidus. This suggests that pericytes are associated with and may contribute to vascular fragility and hemodynamic changes in bAVMs. Future studies in animal models are needed to better characterize the role of pericytes in AVM pathogenesis.