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BOLD and DTI for Presurgical Mapping

BOLD and DTI for Presurgical Mapping. Jay J. Pillai , M.D. Director of Functional MRI Associate Professor Neuroradiology Division The Russell H. Morgan Department of Radiology and Radiological Science Johns Hopkins Univ. School of Medicine.

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BOLD and DTI for Presurgical Mapping

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  1. BOLD and DTI for Presurgical Mapping Jay J. Pillai, M.D. Director of Functional MRI Associate Professor Neuroradiology Division The Russell H. Morgan Department of Radiology and Radiological Science Johns Hopkins Univ. School of Medicine

  2. What is the purpose of presurgical mapping? Why fMRI & DTI? • Preop risk assessment • Planning surg trajectory • Planning intraop mapping • Eloquent cortex & eloquent WM---goal of neurosurgery • Added value—patient interactive (H & P, training, education prescan), very different from volunteer research scanning

  3. Typical Language Paradigms • Expressive Language Tasks • Verbal Fluency/Phonemic Fluency • Rhyming (Phonological) • Object Naming • Receptive Language Tasks • Sentence Comprehension (V/A)/Story Listening • Sentence Completion • Semantic Decision (category, nva, s/a)

  4. Essential vs. Nonessential Activation • Complementary role of intraop mapping • Role of convergent activation • Role of statistical thresholding

  5. Typical Motor Paradigms • Hand Motor • Bilateral simultaneous or alternating R/L hand • AFT, hand clenching, thumb-index apposition • Foot Motor • Toe flexion/extension • Ankle flexion/extension • Face Motor • Tongue movement—lateral or vertical • Lip puckering

  6. Classical Brodmann’sareas From Waxman SG. Correlative Neuroanatomy, 24th Ed. Lange Medical Books/McGraw-Hill, New York, 2000.

  7. Diffusion Tensor Imaging—Eloquent White Matter is just as important as Eloquent Cortex • Damage to eloquent white matter similar to resection of eloquent cortex • Water molecule diffusion is directionally dependent—anisotropy • The direction of maximum diffusivity coincides with the WM fiber tract orientation

  8. The Diffusion Tensor • The “diffusion tensor”is a matrix of numbers (mathematical model describing diffusion in 3D space) derived from diffusion measurements in several different directions (6+ directions for diffusion encoding). • This tensor depicted as ellipsoid whose orientation is described by three eigenvectors and its shape by three eigenvalues, which are its dimensions (corresponding to diffusivity in each direction).2 1,2 Jellison BJ, Field AS, Medow J, Lazar M, Salamat MS, Alexander AL. Diffusion tensor imaging of cerebral white matter: a pictorial review of physics, fiber tract anatomy, and tumor imaging patterns. AJNR Am J Neuroradiol. 2004 Mar;25(3):356-69

  9. Additional white matter tracts—sagittaltractograms Inferior Fronto-Occipital Fasciculus Arcuate Fasciculus—important for language function/SLF Superior Fronto-Occipital Fasciculus Normal SLF Adapted from Brian J. Jellison, Aaron S. Field, Joshua Medow, Mariana Lazar, M. Shariar Salamat, and Andrew L. Alexander. Diffusion Tensor Imaging of Cerebral White Matter: A Pictorial Review of Physics, Fiber Tract Anatomy, and Tumor Imaging Patterns. AJNR Am. J. Neuroradiol. 2004; 25: 356 - 369. Inferior Longitudinal Fasciculus

  10. SLF • 4 parts of SLF: • SLF I---horizontal fibers connecting superior parietal lobe to frontal/opercular regions (premotor areas and SMA) • SLF II---horizontal fibers connecting the AG to posterior prefrontal cortices • SLF III---horizontal fibers connecting the SMG to F lobe (pars opercularis /ventral premotor areas [BA 44] and ventral prefrontal area [BA 46]) • SLF IV---AF--- connects STG/MTG to frontal regions (caudal dorsal prefrontal cortex, precentralgyrus but not BA as previously thought) Bernal B, Altman N. The connectivity of the superior longitudinal fasciculus: a tractography DTI study. Magnetic Resonance Imaging 28 (2010) 217–225. Schmahmann JD, Pandya DN, Wang R, Dai G, Darceuil HE, de Crespigny AJ, Wedeen VJ. Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 2007; 130:630-653.

  11. Functions of the SLF components • SLF I: higher order control of body-centered action based on proprioception and initiation of motor activity • SLFII: involved in focusing spatial attention (hemi-inattention/neglect w lesions) • SLF III: involved in the gestural component of language and orofacial working memory (lesions result in cortical dysarthria, oral/buccalapraxias, impaired working memory) • SLF IV (AF): thought that lesions result in conduction aphasia, but primate evidence suggests that ExC and MdLF rather than AF responsible; AF actually involved in spatial processing in the auditory domain (indicating location and directionality of sounds rather than symbolic repres of lang) Schmahmann JD, Pandya DN, Wang R, Dai G, Darceuil HE, de Crespigny AJ, Wedeen VJ. Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 2007; 130:630-653.

  12. Martino J, De Witt Hamer PC, Berger MS, Lawton MT, Arnold CM, de Lucas EM, Duffau H. Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study. Brain StructFunct. 2012 Mar 16.

  13. Functions of various other important eloquent tracts • 1) SFOF—responsible for initiation and preparation of speech movements and limbic aspects of speech • 2) IFOF—involved in language ventral stream (semantic network, distinct from phonological network mediated by SLF) • 3) ILF—role in ventral visual stream (object recognition, discrimination and memory including facial recognition—lesion>>>prosopagnosia)—actually lateral to SS • 4) Uncinate fasciculus– processing novel information, understanding emotional aspects of sounds, regulation of emotional responses to auditory stimuli, enables interaction between emotion and cognition, self-regulation, retrieval of past information • 5) Cingulum bundle—dorsal limbic pathway linking caudal cingulategyrus with HC and PHG (memory), prefrontal areas 9 & 46 (manipulating info, monitoring behavior, working memory)—critical for motivational and emotional aspects of behavior, spatial working memory (cingulotomy for OCD) Schmahmann JD, Pandya DN, Wang R, Dai G, Darceuil HE, de Crespigny AJ, Wedeen VJ. Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 2007; 130:630-653. Aralasmak A, Ulmer JL, Kocak M, Salvan CV, Hillis AE, Yousem DM. Association, Commissural and Projection Pathways and Their Functional Deficit Reported in Literature. J Comput Assist Tomogr 2006; 30:695-715.

  14. DTT Validation: Bello et al. Neuroimage 2008 • Study of 52 pts w LGG and 12 w HGG • There was a high correlation between DT-FT and ISM(sensitivity for CST=95%, language tracts=97%). • The combination of both methods decreased the duration of surgery, patient fatigue, and intraoperative seizures. Bello L, Gambini A, Castellano A, et al. Motor and language DTI Fiber Tracking combined with intraoperative subcortical mapping for surgical removal of gliomas. Neuroimage. 2008 Jan 1;39(1):369-82. Epub 2007 Aug 29

  15. Limitations of DTT Bürgel U, Mädler B, Honey CR, Thron A, Gilsbach J, Coenen VA.Fiber tracking with distinct software tools results in a clear diversity in anatomical fiber tract portrayal.Cen Eur Neurosurg. 2009 Feb;70(1):27-35. • 4 different DTT software packages for display of CST of a single normal subject; 3 used FACT (Fiber Assignment by Continuous Tracking) method, one used Tensorline Propagation Algorithm. • None of the software applications was able to display the CST in its full anatomical extent • The 4 packages did not lead to comparable tracking results despite use of similar or identical tracking algorithms

  16. Clinical Value of DTT vs. color directional diffusion maps • DTT is excellent for isolating tracts that run alongside other parallel tracts • Major limitation for clinical use is undersampling of the tract ---operator-dependent seeding, anatomic distortion. • FA/angulation thresholds, step sizes arbitrary • Error propagation—1stvs 2nd order processing • Numerous algorithms---deterministic (discrete, subvoxel) & probabilistic DTT with very little validation

  17. Validation of fMRI: studies comparing fMRI to Wada and ECS results: FROM: Pillai JJ, Language fMRI IN Holodny AI (Ed), Functional Neuroimaging: A Clinical Approach, 2008, Informa Healthcare (New York, NY)

  18. BOLD validation: Studies comparing preop language fMRI to ECS—Giussani et al., Neurosurgery Jan 2010 Giussani, Carlo; Roux, Frank-Emmanuel; MD, PhD; Ojemann, Jeffrey; Sganzerla, Erik; Pirillo, David; Papagno, Costanza Is Preoperative Functional Magnetic Resonance Imaging Reliable for Language Areas Mapping in Brain Tumor Surgery? Review of Language Functional Magnetic Resonance Imaging Neurosurgery. 66(1):113-120, January 2010. 2

  19. Impact of preopfMRI on surgical planning: Petrella et al., Radiology, Sept. 2006;240:793-802 • Functional MRI performed on39 consecutive patients with brain tumors. • Change in neurosurgical treatment plans (as a result of preoperative fMRI) occurred in 19 patients (P < .05),with a more aggressive approach recommended after imaging in 18 patients. • Functional MR imaging resulted in reduced surgical time (estimated reduction, 15–60 minutes) in 22 patientswho underwent surgery, a more aggressive resection in six, and a smaller craniotomy in two. • In four patients, sparing of patients from additional testing (e.g., Wada)because of the functional MRI result. Petrella JR, Shah LM, Harris KM et al. Preoperative functional MR imaging localization of language and motor areas: Effect on therapeutic decision making in patents with potentially resectable brain tumors. Radiology. 2006;240:793-802

  20. Impact of preopfMRI on postoperative clinical outcomeRoessler et al. J NeurolNeurosurg Psychiatry 2005 • Twenty two patients with gliomas near motor cortex evaluated with both motor 3T fMRI and intraoperative motor cortex stimulation (MCS). • FMRI motor foci were successfully detected in all patients preoperatively, whereas MCS was possible in only 17 of 22 patients (77.3%).In those 17 patients, 100% agreement was found between MCS and fMRI for localization of primary motor cortex within 10 mm. • Mild to moderate transient neurological deterioration occurred in six patients, and a severe hemiparesis in one. All patients recovered within 3 months(31.8% transient, 0% permanent morbidity). Roessler K, Donat M, Lanzenberger R, Novak K, Geissler A, Gartus A, Tahamtan AR, Milakara D, Czech T, Barth M, Knosp E, Beisteiner R. Evaluation of preoperative high magnetic field motor functional MRI (3 Tesla) in glioma patients by navigated electrocortical stimulation and postoperative outcome. J Neurol Neurosurg Psychiatry. 2005 Aug;76(8):1152-7

  21. Impact of preop DTI on Postsurgical Clinical Outcome Wu JS et al., Neurosurgery 2007 • Studied 238 pts—118 underwent DTI, 120 std 3D struct scans only for neuronavigation. • Postoperative motor deterioration occurred in 32.8% of control cases, compared to 15.3% of the study cases (P < 0.001). • The 6-month Karnofsky Performance Scale score of study cases was significantly higher than that of control cases, P < 0.001; greater difference for HGG than LGG. • For 81 HGGs, the median survival of study cases was 21.2 months compared with 14.0 months of control cases (P = 0.048). Wu JS, Zhou LF, Tang WJ, Mao Y, Hu J, Song YY, Hong XN, Du GH. Clinical evaluation and follow-up outcome of diffusion tensor imaging-based functional neuronavigation: a prospective, controlled study in patients with gliomas involving pyramidal tracts. Neurosurgery. 2007 Nov;61(5):935-48; discussion 948-9

  22. Preop BOLD fMRI may serve as a prognostic indicator—recent paper by Wood et al., AJNR 2011 • 74 patients w primary or met tumor underwent BOLD motor mapping • 77 patients underwent BOLD language mapping • Motor (p<0.001) and lang (P=0.009)LAD signifa/w pre or postop deficits • Pre and postop deficits, grade, tumor loc and LAD predicted mortality • Motor deficits increased linearly as dist from tumor to PSMC decreased, while lang deficits incr exponentially as dist from tumor to lang areas decr below 1 cm. Wood JM, Kundu B, Utter A, et al. Impact of Brain Tumor Location on Morbidity and Mortality: A Retrospective Functional MR Imaging Study. AJNR Am J Neuroradiol 2011; 32(8): 1420-5.

  23. Clinical impact of BOLD fMRI—relationship between LAD and motor/lang deficits Linear relationship (R2=0.99) between distance from the tumor to the area of activation and the existence of motor deficits (red) and an asymptotic relationship (exponential fit, R2=0.88) between the distance from the tumor to the area of activation and the existence of language deficits. Error bars depict 95% CIs calculated for a proportion. Wood JM, Kundu B, Utter A, et al. Impact of Brain Tumor Location on Morbidity and Mortality: A Retrospective Functional MR Imaging Study. AJNR Am J Neuroradiol 2011; 32(8): 1420-5.

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