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Mark A. Rivkin and Steven S. Yocom

Object

Thoracolumbar instrumentation has experienced a dramatic increase in utilization over the last 2 decades. However, pedicle screw fixation remains a challenging undertaking, with suboptimal placement contributing to postoperative pain, neurological deficit, vascular complications, and return to the operating suite. Image-guided spinal surgery has substantially improved the accuracy rates for these procedures. However, it is not without technical challenges and a learning curve for novice operators. The authors present their experience with the O-arm intraoperative imaging system and share the lessons they learned over nearly 5 years.

Methods

The authors performed a retrospective chart review of 270 consecutive patients who underwent thoracolumbar pedicle screw fixation utilizing the O-arm imaging system in conjunction with StealthStation navigation between April 2009 and September 2013 at a single tertiary care center; 266 of the patients underwent CT scanning on postoperative Day 1 to evaluate hardware placement. The CT scans were interpreted prospectively by 3 neuroradiologists as part of standard work flow and retrospectively by 2 neurosurgeons and a senior resident. Pedicle screws were evaluated for breaches according to the 3-tier classification proposed by Mirza et al.

Results

Of 270 patients, 266 (98.5%) were included in the final analysis based on the presence of a postoperative CT scan. Overall, 1651 pedicle screws were placed in 266 patients and yielded a 5.3% breach rate; 213 thoracic and 1438 lumbosacral pedicle screws were inserted with 6.6% and 5.1% breach rates, respectively. Of the 87 suboptimally placed screws, there were 13 Grade 1, 16 Grade 2, and 12 Grade 3 misses as well as 46 anterolateral or “tip-out” perforations at L-5. Four patients (1.5%) required a return to the operating room for pedicle screw revision, 2 of whom experienced transient radicular symptoms and 2 remained asymptomatic. Interestingly, the pedicle breach rate was higher than anticipated at 13.21% for the 30 patients over the initial 6-month period with the O-arm. After certain modifications to the authors' technique, the subsequent 30 patients experienced a statistically significant decrease in breach rate at 5.6% (p = 0.014).

Conclusions

Image-guided spinal surgery can be a great option in the operating room and provides high pedicle screw accuracy rates. With numerous systems commercially available, it is important to develop a systematic approach regardless of the technology in question. There is a learning curve for surgeons unfamiliar with image guidance that should be recognized and appreciated when transitioning to navigation-assisted spinal surgery. In fact, the authors' experience with a large patient cohort suggests that this learning curve may be more significant than previously reported.

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Robert Lynagh, Mark Ishak, Joseph Georges, Danielle Lopez, Hany Osman, Michael Kakareka, Brandon Boyer, H. Warren Goldman, Jennifer Eschbacher, Mark C. Preul, Peter Nakaji, Alan Turtz, Steven Yocom and Denah Appelt

OBJECTIVE

Accurate histopathological diagnoses are often necessary for treating neuro-oncology patients. However, stereotactic biopsy (STB), a common method for obtaining suspicious tissue from deep or eloquent brain regions, fails to yield diagnostic tissue in some cases. Failure to obtain diagnostic tissue can delay initiation of treatment and may result in further invasive procedures for patients. In this study, the authors sought to determine if the coupling of in vivo optical imaging with an STB system is an effective method for identification of diagnostic tissue at the time of biopsy.

METHODS

A minimally invasive fiber optic imaging system was developed by coupling a 0.65-mm-diameter coherent fiber optic fluorescence microendoscope to an STB system. Human U251 glioma cells were transduced for stable expression of blue fluorescent protein (BFP) to produce U251-BFP cells that were utilized for in vitro and in vivo experiments. In vitro, blue fluorescence was confirmed, and tumor cell delineation by fluorescein sodium (FNa) was quantified with fluorescence microscopy. In vivo, transgenic athymic rats implanted with U251-BFP cells (n = 4) were utilized for experiments. Five weeks postimplantation, the rats received 5–10 mg/kg intravenous FNa and underwent craniotomies overlying the tumor implantation site and contralateral normal brain. A clinical STB needle containing our 0.65-mm imaging fiber was passed through each craniotomy and images were collected. Fluorescence images from regions of interest ipsilateral and contralateral to tumor implantation were obtained and quantified.

RESULTS

Live-cell fluorescence imaging confirmed blue fluorescence from transduced tumor cells and revealed a strong correlation between tumor cells quantified by blue fluorescence and FNa contrast (R2 = 0.91, p < 0.001). Normalized to background, in vivo FNa-mediated fluorescence intensity was significantly greater from tumor regions, verified by blue fluorescence, compared to contralateral brain in all animals (301.7 ± 34.18 relative fluorescence units, p < 0.001). Fluorescence intensity measured from the tumor margin was not significantly greater than that from normal brain (p = 0.89). Biopsies obtained from regions of strong fluorescein contrast were histologically consistent with tumor.

CONCLUSIONS

The authors found that in vivo fluorescence imaging with an STB needle containing a submillimeter-diameter fiber optic fluorescence microendoscope provided direct visualization of neoplastic tissue in an animal brain tumor model prior to biopsy. These results were confirmed in vivo with positive control cells and by post hoc histological assessment. In vivo fluorescence guidance may improve the diagnostic yield of stereotactic biopsies.

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Robert Lynagh, Mark Ishak, Joseph Georges, Danielle Lopez, Hany Osman, Michael Kakareka, Brandon Boyer, H. Warren Goldman, Jennifer Eschbacher, Mark C. Preul, Peter Nakaji, Alan Turtz, Steven Yocom and Denah Appelt

OBJECTIVE

Accurate histopathological diagnoses are often necessary for treating neuro-oncology patients. However, stereotactic biopsy (STB), a common method for obtaining suspicious tissue from deep or eloquent brain regions, fails to yield diagnostic tissue in some cases. Failure to obtain diagnostic tissue can delay initiation of treatment and may result in further invasive procedures for patients. In this study, the authors sought to determine if the coupling of in vivo optical imaging with an STB system is an effective method for identification of diagnostic tissue at the time of biopsy.

METHODS

A minimally invasive fiber optic imaging system was developed by coupling a 0.65-mm-diameter coherent fiber optic fluorescence microendoscope to an STB system. Human U251 glioma cells were transduced for stable expression of blue fluorescent protein (BFP) to produce U251-BFP cells that were utilized for in vitro and in vivo experiments. In vitro, blue fluorescence was confirmed, and tumor cell delineation by fluorescein sodium (FNa) was quantified with fluorescence microscopy. In vivo, transgenic athymic rats implanted with U251-BFP cells (n = 4) were utilized for experiments. Five weeks postimplantation, the rats received 5–10 mg/kg intravenous FNa and underwent craniotomies overlying the tumor implantation site and contralateral normal brain. A clinical STB needle containing our 0.65-mm imaging fiber was passed through each craniotomy and images were collected. Fluorescence images from regions of interest ipsilateral and contralateral to tumor implantation were obtained and quantified.

RESULTS

Live-cell fluorescence imaging confirmed blue fluorescence from transduced tumor cells and revealed a strong correlation between tumor cells quantified by blue fluorescence and FNa contrast (R2 = 0.91, p < 0.001). Normalized to background, in vivo FNa-mediated fluorescence intensity was significantly greater from tumor regions, verified by blue fluorescence, compared to contralateral brain in all animals (301.7 ± 34.18 relative fluorescence units, p < 0.001). Fluorescence intensity measured from the tumor margin was not significantly greater than that from normal brain (p = 0.89). Biopsies obtained from regions of strong fluorescein contrast were histologically consistent with tumor.

CONCLUSIONS

The authors found that in vivo fluorescence imaging with an STB needle containing a submillimeter-diameter fiber optic fluorescence microendoscope provided direct visualization of neoplastic tissue in an animal brain tumor model prior to biopsy. These results were confirmed in vivo with positive control cells and by post hoc histological assessment. In vivo fluorescence guidance may improve the diagnostic yield of stereotactic biopsies.

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Joseph Georges, Xiaodong Qi, Xiaowei Liu, Yu Zhou, Eric C. Woolf, Amber Valeri, Zein Al-Atrache, Evgenii Belykh, Burt G. Feuerstein, Mark Preul, Adrienne C. Scheck, Mark Reiser, Trent Anderson, Jonas Gopez, Denah Appelt, Steven Yocom, Jennifer Eschbacher, Hao Yan and Peter Nakaji

OBJECTIVE

Differentiating central nervous system (CNS) lymphoma from other intracranial malignancies remains a clinical challenge in surgical neuro-oncology. Advances in clinical fluorescence imaging contrast agents and devices may mitigate this challenge. Aptamers are a class of nanomolecules engineered to bind cellular targets with antibody-like specificity in a fraction of the staining time. Here, the authors determine if immediate ex vivo fluorescence imaging with a lymphoma-specific aptamer can rapidly and specifically diagnose xenografted orthotopic human CNS lymphoma at the time of biopsy.

METHODS

The authors synthesized a fluorescent CNS lymphoma-specific aptamer by conjugating a lymphoma-specific aptamer with Alexa Fluor 488 (TD05-488). They modified human U251 glioma cells and Ramos lymphoma cells with a lentivirus for constitutive expression of red fluorescent protein and implanted them intracranially into athymic nude mice. Three to 4 weeks postimplantation, acute slices (biopsies, n = 28) from the xenografts were collected, placed in aptamer solution, and imaged with a Zeiss fluorescence microscope. Three aptamer staining concentrations (0.3, 1.0, and 3.0 μM) and three staining times (5, 10, and 20 minutes) followed by a 1-minute wash were tested. A file of randomly selected images was distributed to neurosurgeons and neuropathologists, and their ability to distinguish CNS lymphoma from negative controls was assessed.

RESULTS

The three staining times and concentrations of TD05-488 were tested to determine the diagnostic accuracy of CNS lymphoma within a frozen section time frame. An 11-minute staining protocol with 1.0-μM TD05-488 was most efficient, labeling 77% of positive control lymphoma cells and less than 1% of negative control glioma cells (p < 0.001). This protocol permitted clinicians to positively identify all positive control lymphoma images without misdiagnosing negative control images from astrocytoma and normal brain.

CONCLUSIONS

Ex vivo fluorescence imaging is an emerging technique for generating rapid histopathological diagnoses. Ex vivo imaging with a novel aptamer-based fluorescent nanomolecule could provide an intraoperative tumor-specific diagnosis of CNS lymphoma within 11 minutes of biopsy. Neurosurgeons and neuropathologists interpreted images generated with this molecular probe with high sensitivity and specificity. Clinical application of TD05-488 may permit specific intraoperative diagnosis of CNS lymphoma in a fraction of the time required for antibody staining.