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Jan-Karl Burkhardt, Ethan A. Winkler, George F. Lasker, John K. Yue and Michael T. Lawton

OBJECTIVE

Compressive cranial nerve syndromes can be useful bedside clues to the diagnosis of an enlarging intracranial aneurysm and can also guide subsequent evaluation, as with an acute oculomotor nerve (cranial nerve [CN] III) palsy that is presumed to be a posterior communicating artery aneurysm and a surgical emergency until proven otherwise. The CN VI has a short cisternal segment from the pontomedullary sulcus to Dorello’s canal, remote from most PICA aneurysms but in the hemodynamic pathway of a rupturing PICA aneurysm that projects toward Dorello’s canal. The authors describe a cranial nerve syndrome for posterior inferior cerebellar artery (PICA) aneurysms that associates subarachnoid hemorrhage (SAH) and an isolated abducens nerve (CN VI) palsy.

METHODS

Clinical and radiological data from 106 surgical patients with PICA aneurysms (66 ruptured and 40 unruptured) were retrospectively reviewed. Data from a group of 174 patients with other aneurysmal SAH (aSAH) were analyzed in a similar manner to control for nonspecific effects of SAH. Univariate statistical analysis compared incidence and risk factors associated with CN VI palsy in subarachnoid hemorrhage.

RESULTS

Overall, 13 (4.6%) of 280 patients had CN VI palsy at presentation, and all of them had ruptured aneurysms (representing 13 [5.4%] of the 240 cases of ruptured aneurysms). CN VI palsies were observed in 12 patients with ruptured PICA aneurysms (12/66 [18.1%]) and 1 patient with other aSAH (1/174 [0.1%], p < 0.0001). PICA aneurysm location in ruptured aneurysms was an independent predictor for CN VI palsy on multivariate analysis (p = 0.001). PICA aneurysm size was not significantly different in patients with or without CN VI palsy (average size 4.4 mm and 5.2 mm, respectively). Within the PICA aneurysm cohort, modified Fisher grade (p = 0.011) and presence of a thick cisternal SAH (modified Fisher Grades 3 and 4) (p = 0.003) were predictors of CN VI palsy. In all patients with ruptured PICA aneurysms and CN VI palsy, dome projection and presumed direction of rupture were directed toward the ipsilateral and/or contralateral Dorello’s canal, in agreement with laterality of the CN palsy. In patients with bilateral CN VI palsies, a medial projection with extensive subarachnoid blood was observed near bilateral canals.

CONCLUSIONS

This study establishes a localizing connection between an isolated CN VI palsy, SAH, and an underlying ruptured PICA aneurysm. CN VI palsy is an important clinical sign in aSAH and when present on initial clinical presentation may be assumed to be due to ruptured PICA aneurysms until proven otherwise. The deficit may be ipsilateral, contralateral, or bilateral and is determined by the direction of the aneurysm dome projection and extent of subarachnoid bleeding toward Dorello’s canal, rather than by direct compression.

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Ethan A. Winkler, John K. Yue, Harjus Birk, Caitlin K. Robinson, Geoffrey T. Manley, Sanjay S. Dhall and Phiroz E. Tarapore

OBJECT

Traumatic fractures of the thoracolumbar spine are common injuries, accounting for approximately 90% of all spinal trauma. Lumbar spine trauma in the elderly is a growing public health problem with relatively little evidence to guide clinical management. The authors sought to characterize the complications, morbidity, and mortality associated with surgical and nonsurgical management in elderly patients with traumatic fractures of the lumbar spine.

METHODS

Using the National Sample Program of the National Trauma Data Bank, the authors performed a retrospective analysis of patients ≥ 55 years of age who had traumatic fracture to the lumbar spine. This group was divided into middle-aged (55–69 years) and elderly (≥ 70 years) cohorts. Cohorts were subdivided into nonoperative, vertebroplasty or kyphoplasty, noninstrumented surgery, and instrumented surgery. Univariate and multivariable analyses were used to characterize and identify predictors of medical and surgical complications, mortality, hospital length of stay, ICU length of stay, number of days on ventilator, and hospital discharge in each subgroup. Adjusted odds ratios, mean differences, and associated 95% CIs were reported. Statistical significance was assessed at p < 0.05, and the Bonferroni correction for multiple comparisons was applied for each outcome analysis.

RESULTS

Between 2003 and 2012, 22,835 people met the inclusion criteria, which represents 94,103 incidents nationally. Analyses revealed a similar medical and surgical complication profile between age groups. The most prevalent medical complications were pneumonia (7.0%), acute respiratory distress syndrome (3.6%), and deep venous thrombosis (3%). Surgical site infections occurred in 6.3% of cases. Instrumented surgery was associated with the highest odds of each complication (p < 0.001). The inpatient mortality rate was 6.8% for all subjects. Multivariable analyses demonstrated that age ≥ 70 years was an independent predictor of mortality (OR 3.16, 95% CI 2.77–3.60), whereas instrumented surgery (multivariable OR 0.38, 95% CI 0.28–0.52) and vertebroplasty or kyphoplasty (OR 0.27, 95% CI 0.17–0.45) were associated with decreased odds of death. In surviving patients, both older age (OR 0.32, 95% CI 0.30–0.34) and instrumented fusion (OR 0.37, 95% CI 0.33–0.41) were associated with decreased odds of discharge to home.

CONCLUSIONS

The present study confirms that lumbar surgery in the elderly is associated with increased morbidity. In particular, instrumented fusion is associated with periprocedural complications, prolonged hospitalization, and a decreased likelihood of being discharged home. However, fusion surgery is also associated with reduced mortality. Age alone should not be an exclusionary factor in identifying surgical candidates for instrumented lumbar spinal fusion. Future studies are needed to confirm these findings.

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John K. Yue, Ethan A. Winkler, John F. Burke, Andrew K. Chan, Sanjay S. Dhall, Mitchel S. Berger, Geoffrey T. Manley and Phiroz E. Tarapore

OBJECTIVE

Traumatic brain injury (TBI) in children is a significant public health concern estimated to result in over 500,000 emergency department (ED) visits and more than 60,000 hospitalizations in the United States annually. Sports activities are one important mechanism leading to pediatric TBI. In this study, the authors characterize the demographics of sports-related TBI in the pediatric population and identify predictors of prolonged hospitalization and of increased morbidity and mortality rates.

METHODS

Utilizing the National Sample Program of the National Trauma Data Bank (NTDB), the authors retrospectively analyzed sports-related TBI data from children (age 0–17 years) across 5 sports categories: fall or interpersonal contact (FIC), roller sports, skiing/snowboarding, equestrian sports, and aquatic sports. Multivariable regression analysis was used to identify predictors of prolonged length of stay (LOS) in the hospital or intensive care unit (ICU), medical complications, inpatient mortality rates, and hospital discharge disposition. Statistical significance was assessed at α < 0.05, and the Bonferroni correction (set at significance threshold p = 0.01) for multiple comparisons was applied in each outcome analysis.

RESULTS

From 2003 to 2012, in total 3046 pediatric sports-related TBIs were recorded in the NTDB, and these injuries represented 11,614 incidents nationally after sample weighting. Fall or interpersonal contact events were the greatest contributors to sports-related TBI (47.4%). Mild TBI represented 87.1% of the injuries overall. Mean (± SEM) LOSs in the hospital and ICU were 2.68 ± 0.07 days and 2.73 ± 0.12 days, respectively. The overall mortality rate was 0.8%, and the prevalence of medical complications was 2.1% across all patients. Severities of head and extracranial injuries were significant predictors of prolonged hospital and ICU LOSs, medical complications, failure to discharge to home, and death. Hypotension on admission to the ED was a significant predictor of failure to discharge to home (OR 0.05, 95% CI 0.03–0.07, p < 0.001). Traumatic brain injury incurred during roller sports was independently associated with prolonged hospital LOS compared with FIC events (mean increase 0.54 ± 0.15 days, p < 0.001).

CONCLUSIONS

In pediatric sports-related TBI, the severities of head and extracranial traumas are important predictors of patients developing acute medical complications, prolonged hospital and ICU LOSs, in-hospital mortality rates, and failure to discharge to home. Acute hypotension after a TBI event decreases the probability of successful discharge to home. Increasing TBI awareness and use of head-protective gear, particularly in high-velocity sports in older age groups, is necessary to prevent pediatric sports-related TBI or to improve outcomes after a TBI.

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Ethan A. Winkler, John K. Yue, John F. Burke, Andrew K. Chan, Sanjay S. Dhall, Mitchel S. Berger, Geoffrey T. Manley and Phiroz E. Tarapore

OBJECTIVE

Sports-related traumatic brain injury (TBI) is an important public health concern estimated to affect 300,000 to 3.8 million people annually in the United States. Although injuries to professional athletes dominate the media, this group represents only a small proportion of the overall population. Here, the authors characterize the demographics of sports-related TBI in adults from a community-based trauma population and identify predictors of prolonged hospitalization and increased morbidity and mortality rates.

METHODS

Utilizing the National Sample Program of the National Trauma Data Bank (NTDB), the authors retrospectively analyzed sports-related TBI data from adults (age ≥ 18 years) across 5 sporting categories—fall or interpersonal contact (FIC), roller sports, skiing/snowboarding, equestrian sports, and aquatic sports. Multivariable regression analysis was used to identify predictors of prolonged hospital length of stay (LOS), medical complications, inpatient mortality rates, and hospital discharge disposition. Statistical significance was assessed at α < 0.05, and the Bonferroni correction for multiple comparisons was applied for each outcome analysis.

RESULTS

From 2003 to 2012, in total, 4788 adult sports-related TBIs were documented in the NTDB, which represented 18,310 incidents nationally. Equestrian sports were the greatest contributors to sports-related TBI (45.2%). Mild TBI represented nearly 86% of injuries overall. Mean (± SEM) LOSs in the hospital or intensive care unit (ICU) were 4.25 ± 0.09 days and 1.60 ± 0.06 days, respectively. The mortality rate was 3.0% across all patients, but was statistically higher in TBI from roller sports (4.1%) and aquatic sports (7.7%). Age, hypotension on admission to the emergency department (ED), and the severity of head and extracranial injuries were statistically significant predictors of prolonged hospital and ICU LOSs, medical complications, failure to discharge to home, and death. Traumatic brain injury during aquatic sports was similarly associated with prolonged ICU and hospital LOSs, medical complications, and failure to be discharged to home.

CONCLUSIONS

Age, hypotension on ED admission, severity of head and extracranial injuries, and sports mechanism of injury are important prognostic variables in adult sports-related TBI. Increasing TBI awareness and helmet use—particularly in equestrian and roller sports—are critical elements for decreasing sports-related TBI events in adults.

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John K. Yue, Ethan A. Winkler, Jonathan W. Rick, Hansen Deng, Carlene P. Partow, Pavan S. Upadhyayula, Harjus S. Birk, Andrew K. Chan and Sanjay S. Dhall

Traumatic spinal cord injury (SCI) often occurs in patients with concurrent traumatic injuries in other body systems. These patients with polytrauma pose unique challenges to clinicians. The current review evaluates existing guidelines and updates the evidence for prehospital transport, immobilization, initial resuscitation, critical care, hemodynamic stability, diagnostic imaging, surgical techniques, and timing appropriate for the patient with SCI who has multisystem trauma. Initial management should be systematic, with focus on spinal immobilization, timely transport, and optimizing perfusion to the spinal cord. There is general evidence for the maintenance of mean arterial pressure of > 85 mm Hg during immediate and acute care to optimize neurological outcome; however, the selection of vasopressor type and duration should be judicious, with considerations for level of injury and risks of increased cardiogenic complications in the elderly. Level II recommendations exist for early decompression, and additional time points of neurological assessment within the first 24 hours and during acute care are warranted to determine the temporality of benefits attributable to early surgery. Venous thromboembolism prophylaxis using low-molecular-weight heparin is recommended by current guidelines for SCI. For these patients, titration of tidal volumes is important to balance the association of earlier weaning off the ventilator, with its risk of atelectasis, against the risk for lung damage from mechanical overinflation that can occur with prolonged ventilation. Careful evaluation of infection risk is a priority following multisystem trauma for patients with relative immunosuppression or compromise. Although patients with polytrauma may experience longer rehabilitation courses, long-term neurological recovery is generally comparable to that in patients with isolated SCI after controlling for demographics. Bowel and bladder disorders are common following SCI, significantly reduce quality of life, and constitute a focus of targeted therapies. Emerging biomarkers including glial fibrillary acidic protein, S100β, and microRNAs for traumatic SCIs are presented. Systematic management approaches to minimize sources of secondary injury are discussed, and areas requiring further research, implementation, and validation are identified.

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Ross C. Puffer, John K. Yue, Matthew Mesley, Julia B. Billigen, Jane Sharpless, Anita L. Fetzick, Ava Puccio, Ramon Diaz-Arrastia and David O. Okonkwo

OBJECTIVE

Following traumatic brain injury (TBI), midline shift of the brain at the level of the septum pellucidum is often caused by unilateral space-occupying lesions and is associated with increased intracranial pressure and worsened morbidity and mortality. While outcome has been studied in this population, the recovery trajectory has not been reported in a large cohort of patients with TBI. The authors sought to utilize the Citicoline Brain Injury Treatment (COBRIT) trial to analyze patient recovery over time depending on degree of midline shift at presentation.

METHODS

Patient data from the COBRIT trial were stratified into 4 groups of midline shift, and outcome measures were analyzed at 30, 90, and 180 days postinjury. A recovery trajectory analysis was performed identifying patients with outcome measures at all 3 time points to analyze the degree of recovery based on midline shift at presentation.

RESULTS

There were 892, 1169, and 895 patients with adequate outcome data at 30, 90, and 180 days, respectively. Rates of favorable outcome (Glasgow Outcome Scale–Extended [GOS-E] scores 4–8) at 6 months postinjury were 87% for patients with no midline shift, 79% for patients with 1–5 mm of shift, 64% for patients with 6–10 mm of shift, and 47% for patients with > 10 mm of shift. The mean improvement from unfavorable outcome (GOS-E scores 2 and 3) to favorable outcome (GOS-E scores 4–8) from 1 month to 6 months in all groups was 20% (range 4%–29%). The mean GOS-E score for patients in the 6- to 10-mm group crossed from unfavorable outcome (GOS-E scores 2 and 3) into favorable outcome (GOS-E scores 4–8) at 90 days, and the mean GOS-E of patients in the > 10-mm group nearly reached the threshold of favorable outcome by 180 days postinjury.

CONCLUSIONS

In this secondary analysis of the Phase 3 COBRIT trial, TBI patients with less than 10 mm of midline shift on admission head CT had significantly improved functional outcomes through 180 days after injury compared with those with greater than 10 mm of midline shift. Of note, nearly 50% of patients with > 10 mm of midline shift achieved a favorable outcome (GOS-E score 4–8) by 6 months postinjury.

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Ethan A. Winkler, Jan-Karl Burkhardt, W. Caleb Rutledge, Jonathan W. Rick, Carlene P. Partow, John K. Yue, Harjus Birk, Ashley M. Bach, Kunal P. Raygor and Michael T. Lawton

OBJECTIVE

Shunt-dependent hydrocephalus is an important cause of morbidity following aneurysmal subarachnoid hemorrhage (aSAH) in excess of 20% of cases. Hydrocephalus leads to prolonged hospital and ICU stays, well as to repeated surgical interventions, readmissions, and complications associated with ventriculoperitoneal (VP) shunts, including shunt failure and infection. Whether variations in surgical technique at the time of aneurysm treatment may modify rates of shunt dependency remains a matter of debate. Here, the authors report on their experience with tandem fenestration of the lamina terminalis (LT) and membrane of Liliequist (MoL) at the time of open microsurgical repair of the ruptured aneurysm.

METHODS

The authors conducted a retrospective review of 663 consecutive patients with aSAH treated from 2005 to 2015 by open microsurgery via a pterional or orbitozygomatic craniotomy by the senior author (M.T.L.). Data collected from review of the electronic medical record included age, Hunt and Hess grade, Fisher grade, need for an external ventricular drain, and opening pressure. Patients were stratified into those undergoing no fenestration and those undergoing tandem fenestration of the LT and MoL at the time of surgical repair. Outcome variables, including VP shunt placement and timing of shunt placement, were recorded and statistically analyzed.

RESULTS

In total, shunt-dependent hydrocephalus was observed in 15.8% of patients undergoing open surgical repair following aSAH. Tandem microsurgical fenestration of the LT and MoL was associated with a statistically significant reduction in shunt dependency (17.9% vs 3.2%, p < 0.01). This effect was confirmed with multivariate analysis of collected variables (multivariate OR 0.09, 95% CI 0.03–0.30). Number-needed-to-treat analysis demonstrated that tandem fenestration was required in approximately 6.8 patients to prevent a single VP shunt placement. A statistically significant prolongation in days to VP shunt surgery was also observed in patients treated with tandem fenestration (26.6 ± 19.4 days vs 54.0 ± 36.5 days, p < 0.05).

CONCLUSIONS

Tandem fenestration of the LT and MoL at the time of open microsurgical clipping and/or bypass to secure ruptured anterior and posterior circulation aneurysms is associated with reductions in shunt-dependent hydrocephalus following aSAH. Future prospective randomized multicenter studies are needed to confirm this result.

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Ethan A. Winkler, John K. Yue, Hansen Deng, Kunal P. Raygor, Ryan R. L. Phelps, Caleb Rutledge, Alex Y. Lu, Roberto Rodriguez Rubio, Jan-Karl Burkhardt and Adib A. Abla

OBJECTIVE

Cerebral bypass procedures are microsurgical techniques to augment or restore cerebral blood flow when treating a number of brain vascular diseases including moyamoya disease, occlusive vascular disease, and cerebral aneurysms. With advances in endovascular therapy and evolving evidence-based guidelines, it has been suggested that cerebral bypass procedures are in a state of decline. Here, the authors characterize the national trends in cerebral bypass surgery in the United States from 2002 to 2014.

METHODS

Using the National (Nationwide) Inpatient Sample, the authors extracted for analysis the data on all adult patients who had undergone cerebral bypass as indicated by ICD-9-CM procedure code 34.28. Indications for bypass procedures, patient demographics, healthcare costs, and regional variations are described. Results were stratified by indication for cerebral bypass including moyamoya disease, occlusive vascular disease, and cerebral aneurysms. Predictors of inpatient complications and death were evaluated using multivariable logistic regression analysis.

RESULTS

From 2002 to 2014, there was an increase in the annual number of cerebral bypass surgeries performed in the United States. This increase reflected a growth in the number of cerebral bypass procedures performed for adult moyamoya disease, whereas cases performed for occlusive vascular disease or cerebral aneurysms declined. Inpatient complication rates for cerebral bypass performed for moyamoya disease, vascular occlusive disease, and cerebral aneurysm were 13.2%, 25.1%, and 56.3%, respectively. Rates of iatrogenic stroke ranged from 3.8% to 20.4%, and mortality rates were 0.3%, 1.4%, and 7.8% for moyamoya disease, occlusive vascular disease, and cerebral aneurysms, respectively. Multivariate logistic regression confirmed that cerebral bypass for vascular occlusive disease or cerebral aneurysm is a statistically significant predictor of inpatient complications and death. Mean healthcare costs of cerebral bypass remained unchanged from 2002 to 20014 and varied with treatment indication: moyamoya disease $38,406 ± $483, vascular occlusive disease $46,618 ± $774, and aneurysm $111,753 ± $2381.

CONCLUSIONS

The number of cerebral bypass surgeries performed for adult revascularization has increased in the United States from 2002 to 2014. Rising rates of surgical bypass reflect a greater proportion of surgeries performed for moyamoya disease, whereas bypasses performed for vascular occlusive disease and aneurysms are decreasing. Despite evolving indications, cerebral bypass remains an important surgical tool in the modern endovascular era and may be increasing in use. Stagnant complication rates highlight the need for continued interest in advancing available bypass techniques or technologies to improve patient outcomes.

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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.