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John Y. K. Lee, John T. Pierce, Sukhmeet K. Sandhu, Dmitriy Petrov and Andrew I. Yang

OBJECTIVE

Endoscopic surgery has revolutionized surgery of the ventral skull base but has not yet been widely adopted for use in the cerebellopontine angle. Given the relatively normal anatomy of the cerebellopontine angle in patients with trigeminal neuralgia (TN), the authors hypothesized that a fully endoscopic microvascular decompression (E-MVD) might provide pain outcomes equivalent to those of microscopic MVD (M-MVD) but with fewer complications.

METHODS

The authors conducted a single-institution, single-surgeon retrospective study with patients treated in the period of 2006–2013. Before surgery, all patients completed a questionnaire that included a validated multidimensional pain-outcome tool, the Penn Facial Pain Scale (PFPS, formerly known as Brief Pain Inventory–Facial), an 11-point scale that measures pain intensity, interference with general activities of daily living (ADLs), and facial-specific ADLs. Using a standardized script, independent research assistants conducted follow-up telephone interviews.

RESULTS

In total, 167 patients were available for follow-ups (66.5% female; 93 patients underwent M-MVD and 74 underwent E-MVD). Preoperative characteristics (i.e., TN classification, PFPS components, and medication use) were similar for the 2 surgical groups except for 2 variables. Patients in the M-MVD group had slightly higher incidence of V3 pain, and the 2 groups differed in the date of surgery and hence in the length of follow-up (2.4 years for the M-MVD group and 1.3 years for the E-MVD group, p < 0.05). There was a trend toward not finding neurovascular conflict at the time of surgery more frequently in the M-MVD than in the E-MVD group (11% vs 7%, p = 0.052). Internal neurolysis was more often performed in the E-MVD group (26% vs 7%, p = 0.001). The 2 groups did not significantly differ in the length of the MVD procedure (approximately 2 hours). Self-reported headaches at 1 month postoperatively were present in 21% of the patients in the M-MVD group versus 7% in the E-MVD group (p = 0.01). Pain outcomes at the most recent followup were equivalent, with patients reporting a 5- to 6-point (70%–80%) improvement in pain intensity, a 5-point (85%) improvement in pain interference with ADLs, and a 6-point (85%) improvement in interference with facial-specific ADLs. Actuarial freedom from pain recurrence was equivalent in the 2 groups, with 80% pain control at 3 years.

CONCLUSIONS

Both the fully endoscopic MVD and the conventional M-MVD appear to provide patients with equivalent pain outcomes. Complication rates were also similar between the groups, with the exception of the rate of headaches, which was significantly lower in the E-MVD group 1 month postoperatively.

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Leif-Erik Bohman, John Pierce, James H. Stephen, Sukhmeet Sandhu and John Y. K. Lee

Object

Fully endoscopicmicrovascular decompression (E-MVD) of the trigeminal nerve was initially described more than 1 decade ago, but has not yet gained wide acceptance. The authors present the experience of their first 47 consecutive E-MVDs for trigeminal neuralgia (TN).

Methods

All surgeries were performed by a single surgeon (J.Y.K.L.) at the Pennsylvania Hospital at the University of Pennsylvania. Patients prospectively completed pain scales before and after surgery by using the Brief Pain Inventory–Facial outcomes tool. All patients were called on the telephone, and the same outcome tool was administered without reference to their preoperative pain status.

Results

Forty-seven patients (17 men) were identified and enrolled. Forty (85%) had Burchiel Type 1 TN. Vascular compression was observed at surgery in 42 patients (89%). No surgery was aborted or converted to microscope. One patient suffered permanent hearing loss, for a permanent neurological morbidity rate of 2%. Overall improvement in pain outcomes was excellent, with a median maximum pain intensity preoperatively of 10 and postoperatively of 0 (p< 0.0001). The mean interference with global function scores were 6.2 preoperatively and reduced to 1.0 at last follow-up (p < 0.0001). The mean interference with facial function was 7.3 preoperatively and reduced to 1.2 at last follow-up (p < 0.0001). The mean follow-up period after surgery was 15 ± 8 months.

Conclusions

In experienced hands, E-MVD offers superb visualization and illumination and is both safe and effective, at least in the short term. Further longer-term study is needed to compare E-MVD to traditional microscopic MVD.

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John Y. K. Lee, John T. Pierce, Jayesh P. Thawani, Ryan Zeh, Shuming Nie, Maria Martinez-Lage and Sunil Singhal

OBJECTIVE

Meningiomas are the most common primary tumor of the central nervous system. Complete resection can be curative, but intraoperative identification of dural tails and tumor remnants poses a clinical challenge. Given data from preclinical studies and previous clinical trials, the authors propose a novel method of localizing tumor tissue and identifying residual disease at the margins via preoperative systemic injection of a near-infrared (NIR) fluorescent contrast dye. This technique, what the authors call “second-window indocyanine green” (ICG), relies on the visualization of ICG approximately 24 hours after intravenous injection.

METHODS

Eighteen patients were prospectively identified and received 5 mg/kg of second-window ICG the day prior to surgery. An NIR camera was used to localize the tumor prior to resection and to inspect the margins following standard resection. The signal to background ratio (SBR) of the tumor to the normal brain parenchyma was measured in triplicate. Gross tumor and margin specimens were qualitatively reported with respect to fluorescence. Neuropathological diagnosis served as the reference gold standard to calculate the sensitivity and specificity of the imaging technique.

RESULTS

Eighteen patients harbored 15 WHO Grade I and 3 WHO Grade II meningiomas. Near-infrared visualization during surgery ranged from 18 to 28 hours (mean 23 hours) following second-window ICG infusion. Fourteen of the 18 tumors demonstrated a markedly elevated SBR of 5.6 ± 1.7 as compared with adjacent brain parenchyma. Four of the 18 patients showed an inverse pattern of NIR signal, that is, stronger in the adjacent normal brain than in the tumor (SBR 0.31 ± 0.1). The best predictor of inversion was time from injection, as the patients who were imaged earlier were more likely to demonstrate an appropriate SBR. The second-window ICG technique demonstrated a sensitivity of 96.4%, specificity of 38.9%, positive predictive value of 71.1%, and a negative predictive value of 87.5% for tumor.

CONCLUSIONS

Systemic injection of NIR second-window ICG the day before surgery can be used to visualize meningiomas intraoperatively. Intraoperative NIR imaging provides higher sensitivity in identifying meningiomas than the unassisted eye. In this study, 14 of the 18 patients with meningioma demonstrated a strong SBR compared with adjacent brain. In the future, reducing the time interval from dye injection to intraoperative imaging may improve fluorescence at the margins, though this approach requires further investigation.

Clinical trial registration no.: NCT02280954 (clincialtrials.gov).

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John F. Burke, Jayesh P. Thawani, Ian Berger, Nikhil R. Nayak, James H. Stephen, Tunde Farkas, Hovik John Aschyan, John Pierce, Suhail Kanchwala, Donlin M. Long and William C. Welch

OBJECTIVE

Tarlov cysts (TCs) occur most commonly on extradural components of the sacral and coccygeal nerve roots. These lesions are often found incidentally, with an estimated prevalence of 4%–9%. Given the low estimated rates of symptomatic TC and the fact that symptoms can overlap with other common causes of low-back pain, optimal management of this entity is a matter of ongoing debate. Here, the authors investigate the effects of surgical intervention on symptomatic TCs and aim to solidify the surgical criteria for this disease process.

METHODS

The authors performed a retrospective review of data from consecutive patients who were surgically treated for symptomatic TCs from September 2011 to March 2013. Clinical evaluations and results from surveying pain and overall health were used. Univariate statistical analyses were performed.

RESULTS

Twenty-three adults (4 males, 19 females) who had been symptomatic for a mean of 47.4 months were treated with laminectomy, microsurgical exposure and/or imbrication, and paraspinous muscle flap closure. Eighteen patients (78.3%) had undergone prior interventions without sustained improvement. Thirteen patients (56.5%) underwent lumbar drainage for an average of 8.7 days following surgery. The mean follow-up was 14.4 months. Univariate analyses demonstrated that an advanced age (p = 0.045), the number of noted perineural cysts on preoperative imaging (p = 0.02), and the duration of preoperative symptoms (p = 0.03) were associated with a poor postoperative outcome. Although 47.8% of the patients were able to return to normal activities, 93.8% of those surveyed reported that they would undergo the operation again if given the choice.

CONCLUSIONS

This is one of the largest published studies on patients with TCs treated microsurgically. The data suggest that patients with symptomatic TCs may benefit from open microsurgical treatment. Although outcomes seem related to patient age, duration of symptoms, and extent of disease demonstrated on imaging, further study is warranted and underway.

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David M. Lyle, John P. Pierce, Edward A. Freeman, Roger Bartrop, Nicholas W. C. Dorsch, Michael R. Fearnside, Robin G. Rushworth and John M. F. Grant

✓ The records of 159 severely head-injured patients (all in coma for longer than 6 hours) from Sydney, Australia, were studied. The clinical course, charted over a 2-week period, indicated that 60% of deaths occur by Day 3 and that 12% of patients remain in coma (Glagow Coma Scale (GCS) score < 7) for more than 2 weeks. Overall, at long-term follow-up review more than 2 years after injury, 51% of patients were dead, 7% were severely disabled or vegetative, and 42% had a good to moderate recovery. Outcome of the patients in prolonged coma was assessed separately, with only one-third making a good or moderate recovery; two-thirds of the severely disabled patients came from this group. The high proportion of poor outcomes associated with prolonged coma suggests that this group of patients should be specifically targeted in research. One appropriate intervention with this group would be the restructuring and intensification of early rehabilitation. However, the GCS score lacks the precision needed for this type of study, and a better measure of recovery should be developed.

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Reginald J. Davis, Kee D. Kim, Michael S. Hisey, Gregory A. Hoffman, Hyun W. Bae, Steven E. Gaede, Ralph F. Rashbaum, Pierce Dalton Nunley, Daniel L. Peterson and John K. Stokes

Object

Cervical total disc replacement (TDR) is intended to treat neurological symptoms and neck pain associated with degeneration of intervertebral discs in the cervical spine. Anterior cervical discectomy and fusion (ACDF) has been the standard treatment for these indications since the procedure was first developed in the 1950s. While TDR has been shown to be a safe and effective alternative to ACDF for treatment of patients with degenerative disc disease (DDD) at a single level of the cervical spine, few studies have focused on the safety and efficacy of TDR for treatment of 2 levels of the cervical spine. The primary objective of this study was to rigorously compare the Mobi-C cervical artificial disc to ACDF for treatment of cervical DDD at 2 contiguous levels of the cervical spine.

Methods

This study was a prospective, randomized, US FDA investigational device exemption pivotal trial of the Mobi-C cervical artificial disc conducted at 24 centers in the US. The primary clinical outcome was a composite measure of study success at 24 months. The comparative control treatment was ACDF using allograft bone and an anterior plate. A total of 330 patients were enrolled, randomized, and received study surgery. All patients were diagnosed with intractable symptomatic cervical DDD at 2 contiguous levels of the cervical spine between C-3 and C-7. Patients were randomized in a 2:1 ratio (TDR patients to ACDF patients).

Results

A total of 225 patients received the Mobi-C TDR device and 105 patients received ACDF. At 24 months only 3.0% of patients were lost to follow-up. On average, patients in both groups showed significant improvements in Neck Disability Index (NDI) score, visual analog scale (VAS) neck pain score, and VAS arm pain score from preoperative baseline to each time point. However, the TDR patients experienced significantly greater improvement than ACDF patients in NDI score at all time points and significantly greater improvement in VAS neck pain score at 6 weeks, and at 3, 6, and 12 months postoperatively. On average, patients in the TDR group also maintained preoperative segmental range of motion at both treated segments immediately postoperatively and throughout the study period of 24 months. The reoperation rate was significantly higher in the ACDF group at 11.4% compared with 3.1% for the TDR group. Furthermore, at 24 months TDR demonstrated statistical superiority over ACDF based on overall study success rates.

Conclusions

The results of this study represent the first available Level I clinical evidence in support of cervical arthroplasty at 2 contiguous levels of the cervical spine using the Mobi-C cervical artificial disc. These results continue to support the use of cervical arthroplasty in general, but specifically demonstrate the advantages of 2-level arthroplasty over 2-level ACDF. Clinical trial registration no.: NCT00389597 (ClinicalTrials.gov).

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John Y. K. Lee, Steve S. Cho, Ryan Zeh, John T. Pierce, Maria Martinez-Lage, Nithin D. Adappa, James N. Palmer, Jason G. Newman, Kim O. Learned, Caitlin White, Julia Kharlip, Peter Snyder, Philip S. Low, Sunil Singhal and M. Sean Grady

OBJECTIVE

Pituitary adenomas account for approximately 10% of intracranial tumors and have an estimated prevalence of 15%–20% in the general US population. Resection is the primary treatment for pituitary adenomas, and the transsphenoidal approach remains the most common. The greatest challenge with pituitary adenomas is that 20% of patients develop tumor recurrence. Current approaches to reduce recurrence, such as intraoperative MRI, are costly, associated with high false-positive rates, and not recommended. Pituitary adenomas are known to overexpress folate receptor alpha (FRα), and it was hypothesized that OTL38, a folate analog conjugated to a near-infrared (NIR) fluorescent dye, could provide real-time intraoperative visual contrast of the tumor versus the surrounding nonneoplastic tissues. The preliminary results of this novel clinical trial are presented.

METHODS

Nineteen adult patients who presented with pituitary adenoma were enrolled. Patients were infused with OTL38 2–4 hours prior to surgery. A 4-mm endoscope with both visible and NIR light capabilities was used to visualize the pituitary adenoma and its margins in real time during surgery. The signal-to-background ratio (SBR) was recorded for each tumor and surrounding tissues at various endoscope-to-sella distances. Immunohistochemical analysis was performed to assess the FRα expression levels in all specimens and classify patients as having either high or low FRα expression.

RESULTS

Data from 15 patients (4 with null cell adenomas, 1 clinically silent gonadotroph, 1 totally silent somatotroph, 5 with a corticotroph, 3 with somatotrophs, and 1 somatocorticotroph) were analyzed in this preliminary analysis. Four patients were excluded for technical considerations. Intraoperative NIR imaging delineated the main tumors in all 15 patients with an average SBR of 1.9 ± 0.70. The FRα expression level of the adenomas and endoscope-to-sella distance had statistically significant impacts on the fluorescent SBRs. Additional considerations included adenoma functional status and time from OTL38 injection. SBRs were 3.0 ± 0.29 for tumors with high FRα expression (n = 3) and 1.6 ± 0.43 for tumors with low FRα expression (n = 12; p < 0.05). In 3 patients with immunohistochemistry-confirmed FRα overexpression (2 patients with null cell adenoma and 1 patient with clinically silent gonadotroph), intraoperative NIR imaging demonstrated perfect classification of the tumor margins with 100% sensitivity and 100% specificity. In addition, for these 3 patients, intraoperative residual fluorescence predicted postoperative MRI results with perfect concordance.

CONCLUSIONS

Pituitary adenomas and their margins can be intraoperatively visualized with the preoperative injection of OTL38, a folate analog conjugated to NIR dye. Tumor-to-background contrast is most pronounced in adenomas that overexpress FRα. Intraoperative SBR at the appropriate endoscope-to-sella distance can predict adenoma FRα expression status in real time. This work suggests that for adenomas with high FRα expression, it may be possible to identify margins and to predict postoperative MRI findings.

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Dale Ding, Robert M. Starke, Hideyuki Kano, John Y. K. Lee, David Mathieu, John Pierce, Paul P. Huang, Caleb Feliciano, Rafael Rodriguez-Mercado, Luis Almodovar, Inga S. Grills, Danilo Silva, Mahmoud Abbassy, Symeon Missios, Douglas Kondziolka, Gene H. Barnett, L. Dade Lunsford and Jason P. Sheehan

OBJECTIVE

Because of the angioarchitectural diversity of Spetzler-Martin (SM) Grade III arteriovenous malformations (AVMs), the management of these lesions is incompletely defined. The aims of this multicenter, retrospective cohort study were to evaluate the outcomes after stereotactic radiosurgery (SRS) for SM Grade III AVMs and to determine the factors predicting these outcomes.

METHODS

The authors analyzed and pooled data from patients with SM Grade III AVMs treated with SRS at 8 institutions participating in the International Gamma Knife Research Foundation. Patients with these AVMs and a minimum follow-up length of 12 months were included in the study cohort. An optimal outcome was defined as AVM obliteration, no post-SRS hemorrhage, and no permanently symptomatic radiation-induced changes (RICs). Data were analyzed by univariate and multivariate regression analyses.

RESULTS

The SM Grade III AVM cohort comprised 891 patients with a mean age of 34 years at the time of SRS. The mean nidus volume, radiosurgical margin dose, and follow-up length were 4.5 cm3, 20 Gy, and 89 months, respectively. The actuarial obliteration rates at 5 and 10 years were 63% and 78%, respectively. The annual postradiosurgery hemorrhage rate was 1.2%. Symptomatic and permanent RICs were observed in 11% and 4% of the patients, respectively. Optimal outcome was achieved in 56% of the patients and was significantly more frequent in cases of unruptured AVMs (OR 2.3, p < 0.001). The lack of a previous hemorrhage (p = 0.037), absence of previous AVM embolization (p = 0.002), smaller nidus volume (p = 0.014), absence of AVM-associated arterial aneurysms (p = 0.023), and higher margin dose (p < 0.001) were statistically significant independent predictors of optimal outcome in a multivariate analysis.

CONCLUSIONS

Stereotactic radiosurgery provided better outcomes for patients with small, unruptured SM Grade III AVMs than for large or ruptured SM Grade III nidi. A prospective trial or registry that facilitates a comparison of SRS with conservative AVM management might further clarify the authors' observations for these often high-risk AVMs.

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Mohana Rao Patibandla, Dale Ding, Hideyuki Kano, Zhiyuan Xu, John Y. K. Lee, David Mathieu, Jamie Whitesell, John T. Pierce, Paul P. Huang, Douglas Kondziolka, Caleb Feliciano, Rafael Rodriguez-Mercado, Luis Almodovar, Inga S. Grills, Danilo Silva, Mahmoud Abbassy, Symeon Missios, Gene H. Barnett, L. Dade Lunsford and Jason P. Sheehan

OBJECTIVE

Due to the complexity of Spetzler-Martin (SM) Grade IV–V arteriovenous malformations (AVMs), the management of these lesions remains controversial. The aims of this multicenter, retrospective cohort study were to evaluate the outcomes after single-session stereotactic radiosurgery (SRS) for SM Grade IV–V AVMs and determine predictive factors.

METHODS

The authors retrospectively pooled data from 233 patients (mean age 33 years) with SM Grade IV (94.4%) or V AVMs (5.6%) treated with single-session SRS at 8 participating centers in the International Gamma Knife Research Foundation. Pre-SRS embolization was performed in 71 AVMs (30.5%). The mean nidus volume, SRS margin dose, and follow-up duration were 9.7 cm3, 17.3 Gy, and 84.5 months, respectively. Statistical analyses were performed to identify factors associated with post-SRS outcomes.

RESULTS

At a mean follow-up interval of 84.5 months, favorable outcome was defined as AVM obliteration, no post-SRS hemorrhage, and no permanently symptomatic radiation-induced changes (RIC) and was achieved in 26.2% of patients. The actuarial obliteration rates at 3, 7, 10, and 12 years were 15%, 34%, 37%, and 42%, respectively. The annual post-SRS hemorrhage rate was 3.0%. Symptomatic and permanent RIC occurred in 10.7% and 4% of the patients, respectively. Only larger AVM diameter (p = 0.04) was found to be an independent predictor of unfavorable outcome in the multivariate logistic regression analysis. The rate of favorable outcome was significantly lower for unruptured SM Grade IV–V AVMs compared with ruptured ones (p = 0.042). Prior embolization was a negative independent predictor of AVM obliteration (p = 0.024) and radiologically evident RIC (p = 0.05) in the respective multivariate analyses.

CONCLUSIONS

In this multi-institutional study, single-session SRS had limited efficacy in the management of SM Grade IV–V AVMs. Favorable outcome was only achieved in a minority of unruptured SM Grade IV–V AVMs, which supports less frequent utilization of SRS for the management of these lesions. A volume-staged SRS approach for large AVMs represents an alternative approach for high-grade AVMs, but it requires further investigation.

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Mohana Rao Patibandla, Dale Ding, Hideyuki Kano, Robert M. Starke, John Y. K. Lee, David Mathieu, Jamie Whitesell, John T. Pierce, Paul P. Huang, Douglas Kondziolka, Caleb Feliciano, Rafael Rodriguez-Mercado, Luis Almodovar, Inga S. Grills, Danilo Silva, Mahmoud Abbassy, Symeon Missios, Gene H. Barnett, L. Dade Lunsford and Jason P. Sheehan

OBJECTIVE

The role of and technique for stereotactic radiosurgery (SRS) in the management of arteriovenous malformations (AVMs) have evolved over the past four decades. The aim of this multicenter, retrospective cohort study was to compare the SRS outcomes of AVMs treated during different time periods.

METHODS

The authors selected patients with AVMs who underwent single-session SRS at 8 different centers from 1988 to 2014 with follow-up ≥ 6 months. The SRS eras were categorized as early (1988–2000) or modern (2001–2014). Statistical analyses were performed to compare the baseline characteristics and outcomes of the early versus modern SRS eras. Favorable outcome was defined as AVM obliteration, no post-SRS hemorrhage, and no permanently symptomatic radiation-induced changes (RICs).

RESULTS

The study cohort comprised 2248 patients with AVMs, including 1584 in the early and 664 in the modern SRS eras. AVMs in the early SRS era were significantly smaller (p < 0.001 for maximum diameter and volume), and they were treated with a significantly higher radiosurgical margin dose (p < 0.001). The obliteration rate was significantly higher in the early SRS era (65% vs 51%, p < 0.001), and earlier SRS treatment period was an independent predictor of obliteration in the multivariate analysis (p < 0.001). The rates of post-SRS hemorrhage and radiological, symptomatic, and permanent RICs were not significantly different between the two groups. Favorable outcome was achieved in a significantly higher proportion of patients in the early SRS era (61% vs 45%, p < 0.001), but the earlier SRS era was not statistically significant in the multivariate analysis (p = 0.470) with favorable outcome.

CONCLUSIONS

Despite considerable advances in SRS technology, refinement of AVM selection, and contemporary multimodality AVM treatment, the study failed to observe substantial improvements in SRS favorable outcomes or obliteration for patients with AVMs over time. Differences in baseline AVM characteristics and SRS treatment parameters may partially account for the significantly lower obliteration rates in the modern SRS era. However, improvements in patient selection and dose planning are necessary to optimize the utility of SRS in the contemporary management of AVMs.