- Department of Neurosurgery, Alder Hey Children's NHS Foundation Trust, Liverpool, United Kingdom
- Department of Radiology, Alder Hey Children's NHS Foundation Trust, Liverpool, United Kingdom
Correspondence Address:
Conor L. Mallucci
Department of Neurosurgery, Alder Hey Children's NHS Foundation Trust, Liverpool, United Kingdom
DOI:10.4103/2152-7806.95417
Copyright: © 2012 Yousaf J. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.How to cite this article: Yousaf J, Avula S, Abernethy LJ, Mallucci CL. Importance of intraoperative magnetic resonance imaging for pediatric brain tumor surgery. Surg Neurol Int 26-Apr-2012;3:
How to cite this URL: Yousaf J, Avula S, Abernethy LJ, Mallucci CL. Importance of intraoperative magnetic resonance imaging for pediatric brain tumor surgery. Surg Neurol Int 26-Apr-2012;3:. Available from: http://sni.wpengine.com/surgicalint_articles/importance-of-intraoperative-magnetic-resonance-imaging-for-pediatric-brain-tumor-surgery/
Abstract
Background:High-field intraoperative MRI (IoMRI) is gaining increasing recognition as an invaluable tool in pediatric brain tumor surgery where the extent of tumor resection is a major prognostic factor. We report the initial experience of a dedicated pediatric 3-T intraoperative MRI (IoMRI) unit with integrated neuronavigation in the management of pediatric brain tumors.
Methods:Seventy-three children (mean age 9.5 years; range 0.2–19 years) underwent IoMRI between October 2009 and January 2012, during 79 brain tumor resections using a 3-T MR scanner located adjacent to the neurosurgical operating theater that is equipped with neuronavigation facility. IoMRI was performed either to assess the extent of tumor resection after surgical impression of complete/intended tumor resection or to update neuronavigation. The surgical aims, IoMRI findings, extent of tumor resection, and follow-up data were reviewed.
Results:Complete resection was intended in 47/79 (59%) operations. IoMRI confirmed complete resection in 27/47 (57%). IoMRI findings led to further resection in 12/47 (26%). In 7/47 (15%), IoMRI was equivocal for residual tumor and no evidence of residual tumor was found on re-inspection. In 32/79 (41%) operations, the surgical aim was partial tumor resection. In this subset, surgical resection was extended following IoMRI in 13/32 (41%) operations. None of the patients required early second look procedure for residual disease.
Conclusions:At our institution, IoMRI has led to increased rate of tumor resection and a change in surgical strategy with further tumor resection in 32% of patients. While interpreting IoMRI, it is important to be aware of the known pitfalls.
Keywords: Magnetic resonance imaging, neuronavigation, pediatric brain tumor
INTRODUCTION
Brain tumors are a major cause of mortality and long-term morbidity in the pediatric population. Surgery is a vital part of management, and the degree of primary surgical resection is a major prognostic factor in several tumor types, including the more common malignant tumors such as medulloblastoma, high-grade glioma, and ependymoma.[
High-field intraoperative MRI (IoMRI) is rapidly developing as an aid to safe and effective neurosurgery. The use of neuronavigation systems and operating microscopes is well established in aiding tumor resection. Whilst the role of IoMRI is well documented in adult neurooncology practice, there is limited published literature on its role in the management of pediatric neurosurgical management.
HIGH-FIELD IOMRI FACILITY: DESIGN AND SAFETY CONSIDERATIONS
The IoMRI system at Alder Hey Children's Hospital involves a two-room solution which allows independent function of individual components. It is equipped with a Philips Achieva® 3-T scanner (Philips Healthcare, Best, the Netherlands) with a length of 157 cm and an inner bore of 65 cm. The facility design allows for diagnostic MRI when not needed for IoMRI, making the facility economically viable and allowing for optimal use of this expensive technology. The IoMRI suite is located next to the neurosurgical operating theater, separated by double doors. This arrangement enables independent use of the neurosurgical operating theater and the MRI scanner when IoMRI is not needed.
Special coils and hardware are necessary to facilitate maintenance of sterility of the operative field. IoMRI can be performed using the standard Philips parallel imaging FLEX L coil, with a carbon fiber head clamp, but optimal results are obtained with a dedicated intraoperative head coil (NORAS MRI Products, Hochberg, Germany). The NORAS 8-channel intraoperative head coil contains an integral head clamp with five fixation points (titanium pins) and 14 fiducial markers, allowing accurate intraoperative updating of neuronavigation with automatic registration. Safe transfer of the patient into the MRI scanner is achieved by an MRI-compatible patient transfer table (Maquet, Rastatt, Germany), which docks securely with the MRI platform.
IoMRI poses certain challenges in terms of safe use, both for the theater staff and for the anesthetized patient. The general safety and anesthetic considerations for IoMRI are outlined in Boxes
ALDER HEY EXPERIENCE WITH IoMRI
MATERIALS AND METHODS
Patients
Between October 2009 and January 2012, IoMRI was performed on 73 patients during 79 cranial tumor resections. The mean age was 9.5 years (range 0.2–19 years).
Imaging
IoMRI was performed on a Philips Achieva 3-T scanner (
The surgical aim (complete, subtotal, near-total resection) was defined preoperatively by a multidisciplinary team. The indications of IoMRI have been summarized in
The intraoperative imaging sequences were tailored to tumor characteristics and surgical aims. Standard IoMRI sequences performed at our institution are summarized in
IoMRI was limited to the precontrast sequences if there was unequivocal evidence of residual tumor. The IoMRI scan served as the early postoperative MRI if the IoMRI revealed complete tumor resection or satisfactory degree of subtotal/near-total resection. Repeat IoMRI was performed if further tumor resection was performed after the first IoMRI. Gadopentetate dimeglumine (Magnevist®; Schering, Berlin, Germany) at 0.2 ml/kg bodyweight was used as contrast agent during IoMRI if the tumors demonstrated enhancement on preoperative imaging. The majority of the children received only one dose of contrast during the first and only IoMRI study. The duration of the IoMRI varied between 10 min for a limited study to update neuronavigation and 40 min for a complete early postoperative study.
The IoMRI interpretation was performed by the operating neurosurgeon and a pediatric neuroradiologist in consensus. If the IoMRI findings led to further tumor resection, tissue samples were obtained for histopathologic analysis.
Following the IoMRI, the patient is transferred back to the operating theater, where the images are immediately available to the neurosurgeon using advanced multimodal image display technology.
This study was approved by the research department of our institution as a service evaluation, as defined by the United Kingdom National Patients Safety Agency.
RESULTS
IoMRI was used during 79 cranial tumor resections in 73 children. Overall, IoMRI scan led to further surgery in 25 cases (32%). The results are summarized in
Complete resection intended
Complete surgical resection [Figures
Partial resection intended
Partial resection [Figures
Figure 2a
Sagittal T1-weighted, Gadolinium-enhanced preoperative MRI image showing an enhancing suprasellar mass (histology confirmed it as pilocytic astrocytoma, WHO Grade 1) extending superiorly into the third ventricle and posteriorly between the cerebral peduncles. There is thickening of the optic chiasm
Follow-up
Since the use of IoMRI facility at Alder Hey, there has been no avoidable early second look procedure for residual disease within 1 year of surgery.
DISCUSSION
IoMRI has become increasingly important as a tool to aid safe and complete resection of brain tumors in adults, and is expected to make a major contribution to neurosurgery for pediatric brain tumors. In a study of adults with low-grade gliomas, Pamir et al. have reported that 3-T IoMRI led to further resection in up to 40% of cases and increased the proportion of complete tumor resections by over 30%.[
Other than high-field MRI, other modalities for intraoperative brain imaging include ultrasound (US), computed tomography (CT; using either fixed or mobile scanners), and low- and medium-field MRI. Their relative merits and demerits are discussed in
A dedicated pediatric 3-T IoMRI facility has a number of advantages and challenges. In our initial experience with IoMRI, it has positively influenced our neurosurgical outcome and practice, in particular, the way in which we perform surgery and evaluate our surgical results.
The extent of resection is an important predictor of prognosis in children with medulloblastoma, ependymoma, and high-grade glioma.[
In our experience, high-field IoMRI has not only improved the percentage of gross total resection in keeping with the surgical goal, but also proven invaluable in the surgical management of deep-seated tumors in eloquent areas where the surgical goal had been limited resection. In 41% of our patients where the surgical goal was subtotal resection, further resection was carried out following IoMRI. This is particularly relevant in surgical management of deep-seated chiasmatic/hypothalamic gliomas where a midline approach (transcallosal interforniceal) gives a minimally invasive but limited view of often very large tumors. In these cases, a planned IoMRI [Figures
IoMRI has not only reduced the need for early reoperation, but also reduced the number of early postoperative MRI scans, previously performed routinely between 24 and 48 h post surgery. In our practice, the final IoMRI scan has replaced the postoperative MRI scan and helped to streamline patient care pathway.
Evaluation of IoMRI studies pose certain challenges, and although we have not encountered significant problems with interpretation of IoMRI, they are well described in literature. These include susceptibility artifacts, surgically induced contrast enhancement, and brain shift.
Susceptibility artifact can occur from external sources including metallic objects (even if nominally MRI compatible) such as head holder pins and endotracheal tubes or intracranial sources including hemorrhage and air introduced during surgery. Gradient- and echo planar-sequences are the most affected. The use of titanium pins to hold the head minimizes susceptibility artifact. Also, the pins are usually placed away from the region of interest to minimize the influence of susceptibility artifact on image interpretation. Placing the cuff of the endotracheal tube on the chest rather than beside the head can reduce the associated artifact. Irrigation of surgical cavity reduces the amount of intracranial and intracavitary air.
Surgically induced contrast enhancement is a potential cause for misinterpretation during brain tumor resection. The following four types of contrast enhancement induced by surgery have been described:[
meningeal enhancement, increased enhancement of the choroid plexus, delayed enhancement of the surgical margin, and immediate intraparenchymal enhancement.
The latter two are thought to be caused by leakage of contrast material from surgically open vessels or transient blood brain barrier disruption and have a greater potential to be misinterpreted as residual tumor. This phenomenon is particularly important in tumors with cystic components and at a site where a bipolar cauterizing instrument has been used during surgery. Careful comparison with preoperative imaging is advisable in these circumstances.
Intraoperative brain tissue deformation (brain shift) [Figures
Advances in multimodal neuronavigation have enabled the neurosurgeon's view through the operating microscope to be fused with MR images that may include diffusion tensor imaging (DTI) and functional imaging (Brain-LAB). For reliable tumor resection, a high degree of accuracy is essential for neuronavigation. Brain shift and registration errors are the major factors that may impair navigation accuracy if navigation is based on preoperative MRI. Further inaccuracies can be introduced if the head moves within the holding pins after registration. Progressive brain shift occurs as the bulk of the tumor decreases during the operation. In this situation, neuronavigation based on preoperative MRI may be misleading and potentially dangerous. Updating the navigation system with IoMRI is the most reliable method to overcome these problems. Our use of sophisticated automatic registration systems allows navigation update without using the original patient registration, thereby providing a straightforward and time-efficient method to compensate for brain shift and registration errors. Also, microscope-based image fusion and display can be used for precise localization of residual tumor and orientation within the resection cavity. Advanced display technology with superimposition of the operating microscope image with preoperative and IoMRI facilitates image interpretation.
Without automatic registration techniques, after acquiring new images, the accuracy of intraoperative updating is valid only if there is no positional shifting impairing the initial patient registration. In clinical practice, this can be avoided by taking proven landmark checks just after the first registration. After updating, a side-by-side display of preoperative and intraoperative images of the tumor remnant detection is possible, facilitating orientation, image interpretation, and evaluation of brain shift. In our experience, automatic re-registration, bespoke coils, and attached reference frames have improved speed, accuracy, and reliability.
Our initial results have been encouraging and further research is required to evaluate the clinical effectiveness of IoMRI in the management of specific tumors and the role of advanced MRI techniques in the intraoperative context.
CONCLUSION
In our experience, when managing children, the IoMRI provides us with the ability to illustrate, document, and discuss all aspects of surgery and is a significant improvement in the quality of patient care. Being able to confirm the achievement of surgical aims immediately after surgery is an immeasurable quality leap in parent satisfaction and experience. This technology has transformed our management approach to brain tumor in children by influencing surgical decisions and increasing the rate of complete tumor resection and the extent of partial tumor resection. Optimal use of this expensive intraoperative facility requires careful planning and management. Equivocal findings resulting from postsurgical contrast enhancement can pose challenges. Further studies involving larger numbers of patients/procedures, outcome, and the use of advanced IoMRI techniques need to be encouraged.
Publication of this manuscript has been made possible by an educational grant from
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