Platinum-iridium Sub-dermal Needle Electrodes MRI-compatible Are ...

INSTRUMENTATION AND TECHNIQUE

Platinum-Iridium Subdermal Magnetic Resonance Imaging-Compatible Needle Electrodes Are Suitable for Intraoperative Neurophysiological Monitoring During Image-Guided Surgery With High-Field Intraoperative Magnetic Resonance Imaging: An Experimental Study

Received, December 27, 2013. Accepted, May 9, 2014. Published Online, May 27, 2014.

BACKGROUND: Neurosurgery aims to achieve maximal tumor resection while preserving neurological function. Tools such as neuronavigation, high-field intraoperative magnetic resonance imaging (iMRI), and intraoperative neurophysiological monitoring (IOM) have consistently helped to achieve this goal, but integration has often been difficult. Surgery of eloquent areas requires IOM, which in an operating theater equipped with high-field (1.5-T) iMRI could present several issues. OBJECTIVE: To identify the electrodes types more suitable for IOM in a high-field iMRI operating theater by performing an experimental study on phantoms, to report our experience with platinum-iridium (Pt/Ir) electrodes during surgery, and to prove that integration between IOM with Pt/Ir electrodes and high-field iMRI is safe and reliable. METHODS: Electrodes of different materials (gold, Pt/Ir, and stainless steel) were tested on jelly phantom and apples to evaluate their safety and compatibility. Subsequently, electrodes were tested on 5 healthy volunteers before being used on patients. RESULTS: None of the different electrodes presented thermal instability, and no damage to the volunteers’ skin occurred. Stainless steel electrodes caused severe imaging distortion. Gold electrodes had no distortion, but their high cost makes their use in routine surgery unaffordable. Pt/Ir electrodes are significantly less expensive than gold electrodes and were completely safe, compatible, and suitable for use in an operating theater with high-field iMRI, providing excellent IOM and mild interference that did not affect the quality of intraoperative imaging. CONCLUSION: We suggest the use of Pt/Ir electrodes for IOM in 1.5-T iMRI suites.

Copyright © 2014 by the Congress of Neurological Surgeons.

KEY WORDS: Brain tumors, Intraoperative MRI, Intraoperative neurophysiological monitoring, Platinum-iridium electrodes

Giancarlo D’Andrea, MD* Albina Angelini, MD* Camillo Foresti, MD‡ Pietro Familiari, MD* Emanuela Caroli, MD* Alessandro Frati, MD§ *Neurosurgery, Department of NESMOS, Faculty of Medicine and Psychology and §Neurosurgery, IRCCS Neuromed Pozzilli (Is), University of Rome—Sapienza, Rome, Italy; ‡Department of Neurology, Unit of Neurophysiopathology, Papa Giovanni XXIII Hospital, Bergamo, Italy Correspondence: Giancarlo D’Andrea, MD, V.L. Mantegazza 8, 00152 Roma, Italy. E-mail: [email protected]

Operative Neurosurgery 10:387–392, 2014

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odern neurosurgery aims to achieve maximal tumor resection while preserving neurological function. Over the last decades, new technological tools such as neuronavigation, low-field and high-field intraoperative magnetic resonance imaging (iMRI) with advanced techniques of neuroimaging (diffusion ABBREVIATIONS: DTI, diffusion tensor imaging; iMRI, intraoperative magnetic resonance imaging; IOM, intraoperative neurophysiological monitoring

OPERATIVE NEUROSURGERY

DOI: 10.1227/NEU.0000000000000432

tensor imaging technique [DTI]), and intraoperative neurophysiological monitoring (IOM) have consistently helped to achieve this goal, but their integration has often been difficult. IOM provides a reliable assessment of intraoperative functional changes of the neuronal systems and white matter bundles eventually occurring during surgery, and high-field iMRI can provide imaging of tumor residual and both shifting and morphological changes in functional pathways (by means of DTI) during tumor removal.

VOLUME 10 | NUMBER 3 | SEPTEMBER 2014 | 387

Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited.

D’ANDREA ET AL

Surgery of tumors involving eloquent areas such as brainstem and cerebellopontine angle requires IOM, which in an operating theater with a high-field (1.5-T) iMRI such as the BrainSuite could present several issues such as safety, distortion, and impaired reliability for interferences between IOM and the magnet. This topic is not completely novel.1-3 Szelènyi et al1 already described the successful use of platinum/iridium electrodes for IOM in a low-field (0.15-T) iMRI system, whereas Hatiboglu et al2 suggested that IOM can be safely and successfully combined with high-field iMRI in patients affected by glioma even if no information about the metallic compound of the needles has been provided. Hence, to identify the electrodes types more suitable for IOM in a high-field iMRI operating theater, we performed an experimental study on phantoms. Subdermal needle electrodes of different metallic compounds (gold, platinum/iridium alloy, and stainless steel) believed to be suitable for IOM in the iMRI suite were selected and tested. The aim of this study is to evaluate the interferences between IOM and high-field iMRI and to demonstrate which are the most convenient electrodes to use in terms of safety, costs, and compatibility. Subsequently, we reported our experience with platinumiridium electrodes during surgery of brain tumors in the BrainSuite to prove that in this environment the integration between IOM and high-field iMRI with intraoperative advanced techniques of neuroimaging (DTI) is safe, effective, reliable, and economically affordable.

METHODS Our study was carried out in our institutional operating theater, the BrainSuite iMRI provided by Brainlab, endowed with a 1.5-T scanner, located at the University of Rome “La Sapienza”-affiliated hospital Sant’Andrea. Our study began with an experimental examination of a selection of electrodes believed suitable for use during IOM. The technical tests were carried out with subdermal needle electrodes made of gold, platinum/ iridium alloy, and stainless steel provided by Viasys Healthcare. All electrodes used were disposable hypodermic needles 12 mm in length and 0.4 mm in diameter, with 1.5-m-long cable. Such disposable hypodermic needle electrodes are used for electroencephalography and intensive care monitoring and to stimulate and/or record electrophysiology/ electroencephalography/electromyogram. We carried out tests first on a jelly phantom and then on apples. Next, we checked the electrodes on 5 healthy volunteers (ourselves). Subsequently, those electrodes that were proven to be safe and suitable for IOM in the BrainSuite were used on patients. The jelly phantom was a surgical positioning cylindroid decubitus prevention tool made of semisolid gel provided by Maquet. This phantom has material properties very similar to the cutaneous and subcutaneous tissues (consistency, resistance) to provide compressibility features similar to those of human tissues. Moreover, it has thermal stability and can be used in a temperature range of 212C to 50C. We used an apple as a second phantom to have a tool with a different consistency, geometry, and concentration of H20 molecules. All the different electrodes were positioned at the same time on the phantom and on the apples with a distance of 2 cm between each of them

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with the use of 2 widely separated cables with great care taken to avoid spiral formations, which will lead to increased resistance and hence more image distortion. After these experimental controls, platinum-iridium electrodes were subsequently tested on the feet of 5 healthy volunteers, 2 women and 3 men, during the execution of volumetric and tensor diffusion MRI. The side effects have been measured in terms of thermal modification of the electrodes and of distortion. To register the temperature changes of the electrodes, an MRI-compatible fluoroptic infrared thermometer provided by Luxtron has been used. The fiberoptic probe measured the electrodes temperature in degrees Celsius before and immediately after the MRI. On volunteers and later on patients, we also checked for eventual burning lesion on the placing site (the foot and the scalp, respectively) of the platinum-iridium electrodes. We measured the compatibility of the different electrodes used in the BrainSuite iMRI evaluating the following parameters: image distortion and artifact at the MRI, electrode displacement caused by the highintensity magnetic field, and safety for burning and/or displacement lesions. Distortion had been evaluated in terms of flow void and ghost line and generally on the size of the area of distortion measured in millimeters of each metallic implant on the different models. The distribution of magnetic field varies depending on the positions of the surgical table, so that during surgery the head is placed outside the 5-G line and the IOM equipment is even more distant from the magnet (Figure 1). Cables .7 m long permit the amplifiers and stimulators to be placed on the operating table. IOM is carried out with a set of 4 remote units connected to the central monitoring system (Endeavor, Nimbus Co), two 40-channel recording head boxes, and two 12-channel stimulation boxes. All cables connected to the elements applied to the patient are long enough to run the length of the table and may be easily disconnected when the operating table is moving to acquire an iMRI. The IOM equipment is about 4 to 5 m away from the 5-G line. The amplifiers and stimulators are on the operating table just beyond the 5-G line. The MRI sequences are those applied during ordinary preoperative and intraoperative procedures, in particular, T1 volumetric magnetizationprepared rapid-acquisition gradient-echo (repetition time, 10 780 milliseconds; echo time, 438 milliseconds; field of view, 300; field of view phases, 75), T2 fluid-attenuated inversion-recovery (repetition time, 5680 milliseconds; echo time, 107 milliseconds; field of view, 250; field of view phases, 70), and DTI sequences. After the conclusion of these tests, we performed IOM with platinumiridium subdermal needle electrodes applied on patients’ scalps during surgery for tumors in eloquent areas. Immediately after surgery, all patients were carefully checked to detect scalp burns as potential causality of heated electrodes. iMRI sequences were accurately evaluated to detect eventual paramagnetic artifacts as already specified (area of distortion, flow void, and ghost line). We did not ask for ethical approval for the experimentation on volunteers because we were the volunteers and because platinum-iridium electrodes were purchased with our funds. We sought approval from both the responsible hospital administration and ethics committees, which approved the purchase of the platinum-iridium electrodes and their use in patients affected by lesions in cerebral eloquent areas. All these patients were properly informed of the ongoing clinical experimentation and agreed to sign a specific written consent form.

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IOM IN BRAINSUITE

FIGURE 1. Top, our operating theater, the BrainSuite iMRI provided by Brainlab. Bottom, a schematic drawing of the same theater showing, in relationship to the progressively increasing distance from the magnet, the lines of safety meant to be the magnetic field lines marking the areas of progressive decrease of the magnetic field intensity (10, 5, 3, 1, 0.5 mT). The red line marks the inner boundary of the area with a magnetic field intensity .0.5 mT; hence, surgery is performed outside this area. The ideal positions of the patient, surgeons, anesthesiologists, and assisting nurse and the positions (with a suggested distance of 4-5 m from the patient) of the intraoperative neurophysiological monitoring (IOM) devices and attending neurophysiologist are also schematically suggested in relationship to the above-mentioned lines. An attached rotating table to the magnet allows the patient’s head to be placed outside the 5-G line during surgery. Ordinary surgical instruments can be used outside this line. The IOM equipment is even more distant thanks to 7-m-long cables.

RESULTS The results of the experiments with the different electrodes on the different models are summarized in the Table. All types of electrodes used provided reliable electrophysiological parameters for IOM and proved to be safe in terms of thermal stability. Both gold and platinum-iridium electrodes yielded optimal results, providing reliable IOM, presenting no interference with the magnetic field, and causing no significant artifacts in the iMRI. They were completely compatible with the iMRI and capable of providing excellent IOM in BrainSuite. However, compared with gold electrodes, platinum-iridium electrodes presented some mild distortion of the skin in the placing site (patient’s scalp); however, this did not interfere with the definition of the brain imaging at all. Unfortunately, the prohibitive cost of the gold electrodes excludes their use in routine practice. Stainless steel electrodes demonstrated great distortion of the signal and great interaction with the radiological images, making them incompatible with the iMRI in BrainSuite.


MRI on jelly phantom clearly demonstrated that steel electrodes are in, which does not allow the intraoperative acquisition of advanced techniques of neuroimaging such as DTI. The comparison with platinum-iridium electrodes during the same test dramatically enhanced their difference, providing the intraoperative acquisition of excellent MR signal (Figure 2). The apple test confirmed that the previous findings demonstrated the optimal compatibility of the platinum-iridium electrodes with the intraoperative high magnetic field vs the high rate of artifacts and paramagnetic distortion of the steel electrodes (Figure 3). No significant displacements were observed in any test for every kind of electrode. This observation also demonstrates the feasibility of using stainless steel electrodes in the case of cutaneous needles placed distant from the site of surgery. No burning signs were visible in any kind of electrode, but the infrared thermometer revealed a significant increase in temperature with the use of stainless steel electrodes, proportioned to the time of magnetic exposition. There were no thermic consequences detected with an infrared thermometer or damage to the volunteers’ skin or tissue.



D’ANDREA ET AL

TABLE. Results of the Experiments With the Different Electrodes on the Different Models

Gold Temperature increase Distortion area Flow void Ghost line Platinum-iridium Temperature increase Distortion area Flow void Ghost line Stainless steel Temperature increase Distortion area Flow void Ghost line

Apple

Phantom

Volunteers

Initial temperature = 22.1C (increase, 0.1 6 0.1C) ... ... ...

Initial temperature = 22.0C (increase, 0.2 6 0.3C) ... ... ...

Initial temperature = 22.2 6 0.33C (increase, 0.13 6 0.4C) ... ... ...

Initial temperature = 22.5C (increase, 0.4 6 0.3C)

Initial temperature = 22.3C (increase, 0.3 6 0.1C)

Initial temperature = 22.0 6 0.24C (increase, 0.41 6 0.28C)

2.9 6 0.2 mm · 2.9 6 0.2 mm = 8.41 mm2 Linear Yes



Initial temperature = 22.8C (increase, 0.9 6 0.4C) 16.3 6 3.4 mm · 11.4 6 2.2 mm = 185.82 mm2 Elliptical Yes

Initial temperature = 22.9C (increase, 1.1 6 0.6C) 19 6 4.1 mm · 9.3 6 1.7 mm = 176.7 mm2 Elliptical Yes

Neither paramagnetic interference nor disturbance affecting the quality of the examinations was recorded. Finally, we used platinum-iridium electrodes for IOM in the BrainSuite iMRI for surgery of lesions in eloquent areas (35 gliomas, 11 astrocytomas, 9 oligodendrogliomas, 33 metastases, 23 meningiomas, 15 cranial nerve VIII schwannomas; Figure 4). In all 126 cases operated, no thermic injury occurred. In all instances, it was possible to obtain high-quality intraoperative volumetric and DTI imaging.

In cerebellopontine angle lesions, we acquired constructive interference in steady-state sequences. Again, no artifact influencing the quality of intraoperative images occurred. The ferromagnetic artifacts produced by these electrodes within the 1.5-T field were completely not influent as already seen during the trials carried out before actual in vivo application. The IOM neurophysiological recording apparatus remained constantly outside the 5-G line; this was not impaired in any way, nor did it produce magnetic field disturbances of any kind.

FIGURE 2. The comparison with platinum-iridium electrodes during the jelly phantom test enhanced the difference between stainless steel and platinumiridium, providing the intraoperative acquisition of excellent magnetic resonance imaging (MRI) signal.

FIGURE 3. The apple test confirmed the previous findings demonstrating the optimal compatibility of the platinum-iridium electrodes with the intraoperative high magnetic field vs the high rate of artifacts and paramagnetic distortion of the steel electrodes.




IOM IN BRAINSUITE

FIGURE 4. Intraoperative application in vivo. MRI, magnetic resonance imaging; 3D, 3-dimensional.

Neurophysiological monitoring was carried out to appraise intraoperative motor evoked potentials, phase reversal, free run electromyogram, electroencephalography, electrocorticography, and cranial nerve monitoring. The records were always of the highest quality.

DISCUSSION We have reported our experimental study on different metallic compound electrodes on 3 models to identify the best type of electrodes for IOM during surgery in a high-field iMRI suite. As already pointed out, a perfect integration of these techniques (IOM and iMRI) can improve both surgical aggressiveness and safety during tumor removal in eloquent areas.2 The first issue we tested was safety of the electrodes. The safety of several metallic neurosurgical and of eyelid and middle ear implants under high-field MRI has been proved in different studies to be dependent mainly on the materials used and on the strength of the magnetic field.4-6 When metallic implants are present in the MRI examination, the static magnetic field in their vicinity is manipulated by strong local off-resonances induced by the implants. In general, a high-field scanner produces a specific absorption rate (W/kg) that is much higher than a low field; in the presence of metallic implants, this produces in the nearby area a higher distortion and some increase in temperature. Unlike stainless steel metallic compounds, gold, platinum, and platinum-iridium alloy implants can undergo high-field MRI up to 7.0-T field intensity without any particular risk of heating or dislocation. According to the literature, gold electrodes in a high-field MRI present neither distortion nor an increase in temperature. Platinum and platinum-iridium alloy have higher paramagnetic properties compared with pure gold, which generates no artifacts in a high-field MRI, as evidenced in our experiments. However,


platinum-iridium alloy electrodes have very similar properties in terms of both resistance and thermal stability, presenting in our experience minimal distortion (measured as linear flow void, minimal ghost line, and very small area of distortion) that does not impair the quality of intraoperative neuroimaging, advanced techniques (DTI) included. In fact, electrodes are placed on the scalp, and when used in a high-field scanner, they produce some minimal linear distortion (on humans, about 6.25 mm2) of the nearby skin. This mild distortion does not impair brain imaging at all. Hence, considering the high cost of gold electrodes, platinum-iridium electrodes are an excellent option, as evidenced in our study. On the other hand, stainless steel electrodes, even if presented with a slightly superior increase in temperature, which can be considered safe at 1.5-T iMRI, are still not suitable for this environment because they produced severe distortion that impaired the quality of intraoperative imaging. This was the reason we decided to avoid testing stainless steel electrodes on volunteers. As pointed out earlier, IOM reduces postoperative neurological deficits, improving the quality of therapeutic results. It allows better surgical results combined with a maximum level of surgical aggressiveness indispensable to guarantee a longer illness-free survival7 for lesions of eloquent cortical and subcortical areas. Furthermore, electrocorticography allows us to control cortical excitability, permitting an immediate recognition of the electrical changes preceding intraoperative seizures. We routinely perform IOM during surgery for cortical and subcortical tumors of eloquent areas, acquiring intraoperative volumetric MRI, tractography and constructive interference in steady-state sequences.8 Only 1 study1 involving 29 patients examined the methodological and technical aspects of IOM with platinum-iridium electrodes in a 0.15-T magnetic field. Another article by Hatiboglu et al2 demonstrated how IOM in glioma surgery with high-field iMRI can be safe and feasible. In this study, even if the metallic compound of the electrodes was not specified, the results presented clearly confirm our experience that surgery with IOM in the BrainSuite can achieve more aggressive tumor resection with minimal postoperative deficits. The advantages of a 1.5-T iMRI compared with the lower 0.15-T field are many and of noteworthy importance. It is possible to acquire diffusion-weighted imaging, DTI, angiographic, perfusion, and volumetric sequences in “real-time neuronavigation.” Our results are similar to those presented by Szelènyi et al1 in terms of the safety and effectiveness of platinum-iridium electrodes in an intraoperative magnetic field. In our scenario, we operated using a high magnetic field (1.5-T magnet, Magnetom Sonata, Siemens, Erlangen, Germany), but our results confirmed the absolute safety and effectiveness of such electrodes. Platinum-iridium electrodes never affected the quality of intraoperative images, allowing acquisition of sophisticated sequences without artifacts or distortions.



D’ANDREA ET AL

IOM was never affected by the high-field magnetic field, and all of the intraoperative neurophysiological data were reliable. In no case did we record heating effects leading to patients’ skin damage.

CONCLUSION We demonstrated that platinum-iridium electrodes are compatible with the application of IOM in BrainSuite because of the mild interaction with the high magnetic field and their complete safety. In an examination of the signal distortion created by electrodes, it emerged that those made of gold yielded the most satisfactory results, producing no magnetic field interaction and, most important, proved to be totally compatible with BrainSuite. However, their high cost prohibits their use in clinical practice. Electrodes in platinum and iridium compounds, on the other hand, produced little or no interaction with the high-field MRI and caused no thermal damage to the skin. IOM is effective and safe in the high-field (1.5-T) iMRI BrainSuite.

8. D’Andrea G, Angelini A, Romano A, et al. Intraoperative DTI and brain mapping for surgery of neoplasm of the motor cortex and the corticospinal tract: our protocol and series in BrainSuite. Neurosurg Rev. 2012;35(3):401-412.

COMMENTS

T

he article is addressing a very important topic in multimodal neurosurgery. Combining supportive techniques such as intraoperative neurophysiological monitoring methodologies and high-quality intraoperative imaging is of increasing interest in modern neuro-oncological surgical approaches to achieve the best extent of resection possible and to preserve neurological function. Demonstration of safety of those techniques is therefore an important aspect, and this article provides a structural analysis of different investigations dealing with various types of IOM electrodes used in a high-field intraoperative magnetic resonance imaging environment. Safety and quality aspects have already been demonstrated for an open low-field magnetic resonance imaging system by Szelènyi et al1 in 2008. But this article is providing for the first time systematic data for a high field intraoperative environment. Further studies would be needed to analyses the image distortion and safety in larger case series but the article is providing a valuable base for further studies. Kathleen Seidel Andreas Raabe Bern, Switzerland

Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.

REFERENCES 1. Szelènyi A, Gasser T, Seifert V. Intraoperative neurophysiological monitoring in an open low-field magnetic resonance imaging system: clinical experience and technical considerations. Neurosurgery. 2008;63(4 suppl 2):268-276. 2. Hatiboglu MA, Weinberg JS, Suki D, et al. Utilization of intraoperative motor mapping in glioma surgery with high-field intraoperative magnetic resonance imaging. Stereotact Funct Neurosurg. 2010;88(6):345-352. 3. Weingarten DM, Asthagiri AR, Butman JA, et al. Cortical mapping and frameless stereotactic navigation in the high-field intraoperative magnetic resonance imaging suite. J Neurosurg. 2009;111(6):1185-1190. 4. Shellock FG. Metallic neurosurgical implants: evaluation of magnetic field interactions, heating, and artifacts at 1.5-Tesla. J Magn Reson Imaging. 2001;14(3):295-299. 5. Schrom T, Thelen A, Asbach P, Bauknecht HC. Effect of 7.0 Tesla MRI on upper eyelid implants. Ophthal Plast Reconstr Surg. 2006;22(6):480-482. 6. Thelen A, Bauknecht HC, Asbach P, Schrom T. Behavior of metal implants used in ENT surgery in 7 Tesla magnetic resonance imaging. Eur Arch Otorhinolaryngol. 2006;263(10):900-905. 7. Sanai N, Berger MS. Extent of resection influences outcomes for patients with gliomas. Revue Neurologique. 2011;167(10):648-654.


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he authors report their experience of intraoperative neuromonitoring in the environment of an intraoperative 1.5 T MRI scanner. The advantages of both methods in their sole application towards optimized resection for intraoperative MRI and functional preservation for intraoperative neuro-monitoring, as well as their combined use in a low field MRI scanner have been demonstrated. Now, the safe use of intraoperative neuromonitoring extends to a 1.5 T MRI environment. Despite a slight temperature increase, the imaging and neuromonitoring quality are sound. The cogent use of both methods for the benefit of patients is encouraged. The development of intraoperative scan protocols is recommended. Andrea Szelényi Frankfurt, Germany

1. Szelènyi A, Gasser T, Seifert V. Intraoperative neurophysiological monitoring in an open low-field magnetic resonance imaging system: clinical experience and technical considerations. Neurosurgery. 2008;63(4 suppl 2):268-276.

