Preoperative Magnetic Resonance and Intraoperative Ultrasound Fusion Imaging for Real-Time Neuronavigation in Brain Tumor Surgery

Abstract

Purpose: Brain shift and tissue deformation during surgery for intracranial lesions are the main actual limitations of neuro-navigation (NN), which currently relies mainly on preoperative imaging. Ultrasound (US), being a real-time imaging modality, is becoming progressively more widespread during neurosurgical procedures, but most neurosurgeons, trained on axial computed tomography (CT) and magnetic resonance imaging (MRI) slices, lack specific US training and have difficulties recognizing anatomic structures with the same confidence as in preoperative imaging. Therefore real-time intraoperative fusion imaging (FI) between preoperative imaging and intraoperative ultrasound (ioUS) for virtual navigation (VN) is highly desirable. We describe our procedure for real-time navigation during surgery for different cerebral lesions.

Materials and Methods: We performed fusion imaging with virtual navigation for patients undergoing surgery for brain lesion removal using an ultrasound-based real-time neuro-navigation system that fuses intraoperative cerebral ultrasound with preoperative MRI and simultaneously displays an MRI slice coplanar to an ioUS image.

Results: 58 patients underwent surgery at our institution for intracranial lesion removal with image guidance using a US system equipped with fusion imaging for neuro-navigation. In all cases the initial (external) registration error obtained by the corresponding anatomical landmark procedure was below 2 mm and the craniotomy was correctly placed. The transdural window gave satisfactory US image quality and the lesion was always detectable and measurable on both axes. Brain shift/deformation correction has been successfully employed in 42 cases to restore the co-registration during surgery. The accuracy of ioUS/MRI fusion/overlapping was confirmed intraoperatively under direct visualization of anatomic landmarks and the error was < 3 mm in all cases (100 %).

Conclusion: Neuro-navigation using intraoperative US integrated with preoperative MRI is reliable, accurate and user-friendly. Moreover, the adjustments are very helpful in correcting brain shift and tissue distortion. This integrated system allows true real-time feedback during surgery and is less expensive and time-consuming than other intraoperative imaging techniques, offering high precision and orientation.

Zusammenfassung

Ziel: Brain Shift und Gewebeverschiebung während der chirurgischen Entfernung intrakranialer Raumforderungen sind die limitierenden Faktoren bei der Neuronavigation (NN), welche aktuell hauptsächlich präoperative Bilder einsetzt. Ultraschall (US) als Echtzeit-Bildgebung wird bei neurochirurgischen Prozeduren zunehmend angewandt. Vielen Neurochirurgen fehlt aber die US Expertise, da schon in der Ausbildung standarisierte (typisch axiale) CT und MRT Schnittbilder für die Navigation bevorzugt eingesetzt werden und somit die Sicherheit bei der sonografischen Identifikation anatomischer Strukturen fehlt. Daher ist eine intraoperative Echtzeitfusion zwischen präoperativen CT bzw. MRT Bildern und intraoperativem Ultraschall (ioUS) im Rahmen der virtuellen Navigation (VN) außerordentlich wünschenswert. Wir präsentieren hier die bei uns angewandte Methode für die Echtzeitnavigation bei der Entfernung verschiedener Hirntumoren.

Material und Methoden: Wir wandten die Bildfusion mit virtueller Navigation bei der chirurgischen Entfernung von Hirntumoren an. Zum Einsatz kam ein Neuronavigationssystem, welches intraoperative Ultraschallbilder mit präoperativen MRT Bildern in Echtzeit überlagert und zu jedem US Bild simultan die dazu passende ko-planare MRT-Schnittebene anzeigt.

Ergebnisse: Die US-basierte Neuronavigation wurde bei der Operation von 58 Patienten mit Hirntumoren eingesetzt. In allen Fällen war der Fehler der initialen (externen) Registrierung, welche anhand von anatomischen Landmarken erfolgte, unterhalb von 2mm und die Kraniotomie konnte korrekt angesetzt werden. Die Bildqualität des transduralen Ultraschalls war gut und die Läsion konnte bei allen Patienten detektiert und in allen Achsen vermessen werden. Die Korrektur von Brain Shift sowie Gewebeverschiebung gelang erfolgreich in 42 Fällen zur Wiederherstellung der intraoperativen Co-Registrierung. Die Genauigkeit der Überlagerung von ioUS und MRT wurde intraoperativ anhand der Visualisierung anatomischer Landmarken überprüft und der Fehler lag in allen Fällen (100 %) unterhalb von 3mm.

Schlussfolgerung: Neuronavigation mit Hilfe von in präoperative MRT Bilder integrierten intraoperativen US Bildern ist eine zuverlässige, genaue und anwenderfreundliche neue Technologie. Brain Shift und Gewebeverlagerungen können anhand verschiedener Einstellungsmöglichkeiten am System erfolgreich intraoperativ korrigiert werden. Das integrierte System ermöglicht eine intraoperative Überprüfung der Navigation in Echtzeit und ist dabei kostengünstiger und weniger Zeit aufwändig als andere intraoperative Bild-gebende Verfahren, trotzdem aber hoch präzise.

Key words

brain - tumor - surgery - ultrasound - intraoperative

• References

• 1 Orringer DA, Golby A, Jolesz F. Neuronavigation in the surgical management of brain tumors: current and future trends. Expert Rev Med Devices 2012; 9: 491-500
• 2 Dorward NL, Alberti O, Velani B et al. Postimaging brain distortion: magnitude, correlates, and impact on neuronavigation. J Neurosurg 1998; 88: 656-662
• 3 Nimsky C, Ganslandt O, Cerny S et al. Quantification of, visualization of, and compensation for brain shift using intraoperative magnetic resonance imaging. Neurosurgery 2000; 47: 1070-1090
• 4 Stieglitz LH, Fichtner J, Andres R et al. The silent loss of neuronavigation accuracy: a systematic retrospective analysis of factors influencing the mismatch of frameless stereotactic systems in cranial neurosurgery. Neurosurgery 2013; 72: 796-807
• 5 Black PM, Moriarty T, Alexander EIII et al. Development and implementation of intraoperative magnetic resonance imaging and its neurosurgical applications. Neurosurgery 1997; 41: 831-845
• 6 Hammoud MA, Ligon BL, ElSouki R et al. Use of intraoperative ultrasound for localizing tumors and determining the extent of resection: a comparative study with magnetic resonance imaging. J Neurosurg 1996; 84: 737-741
• 7 Unsgaard G, Gronningsaeter A, Ommedal S et al. Brain operations guided by real-time two-dimensional ultrasound: new possibilities as a result of improved image quality. Neurosurgery 2002; 51: 402-412
• 8 Gerganov VM, Samii A, Akbarian A et al. Reliability of intraoperative high-resolution 2D ultrasound as an alternative to high-field strength MR imaging or tumor resection control: a prospective comparative study. J Neurosurg 2009; 111: 512-519
• 9 Pasto ME, Rifkin MD. Intraoperative ultrasound examination of the brain: possible pitfalls in diagnosis and biopsy guidance. J Ultrasound Med 1984; 3: 245-249
• 10 Lindner D, Trantakis C, Renner C et al. Application of intraoperative 3D ultrasound during navigated tumor resection. Minim Invasive Neurosurg 2006; 49: 197-202
• 11 Rasmussen Jr IA, Lindseth F, Rygh OM et al. Functional neuronavigation combined with intra-operative 3D ultrasound: initial experiences during surgical resections close to eloquent brain areas and future directions in automatic brain shift compensation of preoperative data. Acta Neurochir (Wien) 2007; 149: 365-378
• 12 Jung TY, Jung S, Kim IY et al. Application of neuronavigation system to brain tumor surgery with clinical experience of 420 cases. Minim Invasive Neurosurg 2006; 49: 210-215
• 13 Montali G, Solbiati L, Croce F et al. Fine-needle aspiration biopsy of liver focal lesions ultrasonically guided with a real-time probe. Report on 126 cases. Br J Radiol 1982; 55: 717-723
• 14 De Beni S, Macciò M, Bertora F. Multimodality Navigation Tool ‘Navigator’. IMEKO, IEEE, SICE 2nd International Symposium on Measurement, Analysis and Modeling of Human Functions, 1st Mediterranean Conference on Measurement, June 14–16 Genova, Italy: 2004
• 15 Park HJ, Lee MW, Lee MH et al. Fusion imaging-guided percutaneous biopsy of focal hepatic lesions with poor conspicuity on conventional sonography. J Ultrasound Med 2013; 32: 1557-1564
• 16 Crocetti L, Lencioni R, Debeni S et al. Targeting liver lesions for radiofrequency ablation: an experimental feasibility study using a CT-US fusion imaging system. Invest Radiol 2008; 43: 33-39
• 17 Jung EM, Schreyer AG, Schacherer D et al. New real-time image fusion technique for characterization of tumor vascularisation and tumor perfusion of liver tumors with contrast-enhanced ultrasound, spiral CT or MRI: first results. Clin Hemorheol Microcirc 2009; 43: 57-69
• 18 Nakai M, Sato M, Sahara S et al. Radiofrequency ablation assisted by real-time virtual sonography and CT for hepatocellular carcinoma undetectable by conventional sonography. Cardiovasc Interv Radiol 2009; 32: 62-69
• 19 Giesel FL, Mehndiratta A, Locklin J et al. Image fusion using CT, MRI and PET for treatment, planning, navigation and follow up in percutaneous RFA. Exp Oncol 2009; 31: 106-114
• 20 Ross CJ, Rennert J, Schacherer D et al. Image fusion with volume navigation of contrast enhanced ultrasound (CEUS) with computed tomography (CT) or magnetic resonance imaging (MRI) for post-interventional follow-up after transcatheter arterial chemoembolization (TACE) of hepatocellular carcinomas (HCC): preliminary results. Clin Hemorheol Microcirc 2010; 46: 101-115
• 21 Bucholz RD, Yeh DD, Trobaugh J et al. The correction of stereotactic inaccuracy caused by brain shift using an intraoperative ultrasound device. CVRMed-MRCASL 1997; 459-466
• 22 Comeau RM, Sadikot AF, Fenster A et al. Intraoperative ultrasound for guidance and tissue shift correction in image-guided neurosurgery. Med Phys 2000; 27: 787-800
• 23 Schlaier JR, Warnat J, Dorenbeck U et al. Image fusion of MR images and real-time ultrasonography: evaluation of fusion accuracy combining two commercial instruments, a neuronavigation system and a ultrasound system. Acta Neurochir (Wien) 2004; 146: 271-276
• 24 Gonzalez J, Sosa-Cabrera D, Ortega M et al. Ultrasound Based Intraoperative Brain Shift Correction. IEEE Ultrasonics Symposium. Proceedings 2007: 1571
• 25 Prada F, Perin A, Martegani A et al. Intraoperative contrast-enhanced ultrasound for brain tumor surgery. Neurosurgery 2014; 74: 542-552
• 26 Prada F, Mattei L, Del Bene M et al. Intraoperative cerebral glioma characterization with Contrast Enhanced Ultra-Sound. Biomed Res Int 2014; 2014: 484261
• 27 Moiyadi AV. Objective assessment of intraoperative ultrasound in brain tumors. Acta Neurochir 2014; 156: 703-704
• 28 Moiyadi A, Shetty P. Objective assessment of utility of intraoperative ultrasound in resection of central nervous system tumors: A cost-effective tool for intraoperative navigation in neurosurgery. J Neurosci Rural Pract 2011; 2: 4-11
• 29 Selbekk T, Jakola AS, Solheim O et al. Ultrasound imaging in neurosurgery: approaches to minimize surgically induced image artefacts for improved resection control. Acta Neurochir 2013; 155: 973-980
• 30 Le Roux PD, Berger MS, Wang K et al. Low grade gliomas: comparison of intraoperative ultrasound characteristics with preoperative imaging studies. J Neurooncol 1992; 13: 189-198
• 31 Woydt M, Krone A, Becker G et al. Correlation of intra-operative ultrasound with histopathologic findings after tumour resection in supratentorial gliomas – A method to improve gross total tumour resection. Acta Neurochir (Wien) 1996; 138 (12) 1391-1398