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A Protocol Based on the Fiber Dissection Technique Leandro I Jan-Feb 2013 / Vol 4 / ISSUE 1 ISSN : 2229-5097 Surgical Neurology International • Volume 3 • Issue 3 • May-June 2012 • Pages 261-398 OPEN ACCESS Editor-in-Chief: Surgical Neurology International James I. Ausman, MD, PhD For entire Editorial Board visit : University of California, Los http://www.surgicalneurologyint.com Angeles, CA, USA Original Article Reproducibility of quantitative fiber tracking measurements in diffusion tensor imaging of frontal lobe tracts: A protocol based on the fiber dissection technique Leandro I. Dini1,2, Leonardo M. Vedolin3, Debora Bertholdo3, Rafael D. Grando3, Alessandro Mazzola3, Simone A. Dini2, Gustavo R. Isolan2, Jaderson C. da Costa4, Alvaro Campero5 1Neurosurgery, Grupo Hospitalar Conceição (GHC), Porto Alegre, RS, Brazil; 2Neurosurgery, Fundação Hospital Centenário, São Leopoldo, RS, Brazil; 3Neuroradiology, Hospital Moinhos de Vento (HMV), Porto Alegre, RS, Brazil; 4Neurology, Pontifícia Universidade Católica do Rio Grande do Sul (PUCRS), Porto Alegre, RS, Brazil; 5Neurosurgery, Hospital Padilla, Tucumán, Argentina E‑mail: *Leandro I. Dini ‑ [email protected]; Leonardo M. Vedolin ‑[email protected]; Debora Bertholdo ‑ [email protected]; Rafael D. Grando ‑ [email protected]; Alessandro Mazzola ‑ [email protected]; Simone A. Dini ‑ [email protected]; Gustavo R. Isolan ‑ [email protected]; Jaderson C. da Costa ‑ [email protected]; Alvaro Campero ‑ [email protected] *Corresponding author Received: 16 Dectember 12 ­Accepted: 08 March 13 Published: 12 April 13 This article may be cited as: Dini LI, Vedolin LM, Bertholdo D, Grando RD, Mazzola A, Dini SA, et al. Reproducibility of quantitative fiber tracking measurements in diffusion tensor imaging of frontal lobe tracts: A protocol based on the fiber dissection technique. Surg Neurol Int 2013;4:51. Available FREE in open access from: http://www.surgicalneurologyint.com/text.asp?2013/4/1/51/110508 Copyright: © 2013 Dini LI. 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. Abstract Background: Diffusion tensor imaging (DTI)‑based tractography is a noninvasive in vivo method for tracing white matter bundles. This raises possibilities for qualitative and quantitative assessment of the structural organization of tracts. Nevertheless, questions remain about neuroanatomical accuracy, reproducibility for clinical purposes, and accessibility of the best method for broader application. The aim of this study was to combine the fiber dissection technique and tractography to provide more pertinent insight into brain anatomy and, as a result, to test a protocol for reconstruction of six major frontal lobe tracts. Methods: A combination of fiber dissection of formalin‑fixed brain tissue after freezing (Klingler’s technique) and virtual dissection (tractography) was used to develop a protocol to reconstruct major frontal tracts. Apparent diffusion coefficient (ADC), fractional anisotropy (FA), number of voxels (NVO), volume (VOL), number (NTR), and length (LEN) of tracts were evaluated to assess intra‑ and interobserver reproducibility. Statistical reliability was evaluated using intraclass correlation coefficients (ICCs) and the Pearson association coefficient (r). Access this article online The virtual dissection obtained by tractography seemed to reproduce Results: Website: the anatomic knowledge of the white matter tracts obtained through the classic www.surgicalneurologyint.com method. In reliability study, most ICC and r values corresponded at least to large DOI: correlation. The magnitude of correlation was very high (ICC 0.7‑0.9) or almost 10.4103/2152-7806.110508 perfect (ICC 0.9‑1.0) for the FA and ADC measures of every tract studied. Quick Response Code: Conclusion: The DTI protocol proposed herein provided a reliable method for analysis of reconstructed frontal lobe tracts, especially for the FA and ADC variables. Key Words: Anatomy, diffusion tensor imaging, frontal lobe Surgical Neurology International 2013, 4:51 http://www.surgicalneurologyint.com/content/4/1/51 INTRODUCTION MATERIALS AND METHODS Tractography based on diffusion tensor imaging (DTI) has Anatomic study enabled exploration of the white matter in a unique way. Fiber dissection technique (Klingler’s technique) Through mathematical analysis of the diffusion properties The fiber dissection technique involves layered dissection of water molecules in the parenchyma, white matter of the cerebral white matter to reveal the internal bundles can be recreated in three‑dimensional (3D). anatomic organization of the parenchyma. As an This has made actual virtual dissection of the human improvement to this method, Klingler et al. demonstrated brain and structural quantitative analysis of the brain a that, when specimens are frozen, formalin crystals are possibility, which allows the integrity of selected tracts to formed. As they expand, these crystals separate the fibers, be estimated. making dissection easier.[27] This method has been revived Despite the existence of many different applications by contemporary authors and once more presented as for tractography in the neurosciences, no method the best way of learning about the 3D anatomy of the for identifying bundles is uniform across different brain.[8,27] In this study, two adult human brain specimens research projects.[21] Furthermore, even tractography were fixed in a 10% formalin solution for at least atlases are not unanimous [Table 1][4,30,29,7,6,20], in 2 months. The specimens were washed and then frozen particular with relation to three aspects: (1) the at a temperature of −15°C for 1 week. After this period, presence of comparisons between magnetic resonance they were immersed in water until thawed and dissection imaging (MRI)‑recreated bundles and anatomic was begun with the aid of a surgical microscope (6x and dissections, using a specific method;[27] (2) the presence 40x magnification). The anatomical specimens were of reproducibility studies; and (3) the degree of stored immersed in 5% formalin solution between accessibility for general radiologists. The ideal method dissection sessions. is still being sought; that is, one which does not involve manual region of interest (ROI) selection, is not time Dissections were basically performed using wooden consuming, is accessible for both clinical and research spatulas, starting from the lateral surface. As the cortex applications, and identifies tracts in a manner that is is scraped away with the spatula, a difference can be felt automatic, reproducible and faithful to anatomy, even between the consistency of the cortex and underlying when structural damage is present. white matter; the former is porous and friable, whereas the latter is firm and can be peeled away in layers. Currently, anatomical knowledge is still indispensable, Removal of the cortex and successive layers of fibers whether to conceive an atlas or to interpret results. progressively reveals the deeper anatomy. We followed a Therefore, the traditional fundamentals of anatomy, clear and objective guide to the procedure written by Ture acquired with the classical fiber dissection technique, et al.,[27] covering the stages of dissection and intended to have paradoxically become even more relevant for critical revive use of this technique by those studying the subject. judgment of tractography findings. In this study, the fiber dissection technique was used to provide anatomical The most reliable 3D anatomical findings related to knowledge to serve as the foundation for a DTI‑based the tracts were compiled and stored to be used in the virtual dissection and for the development of simplified manual selection of the ROIs during the subsequent protocols for major frontal lobe tracts. The reproducibility work of tract processing on the workstation. In the of these protocols was then tested by raters who had no different regions we selected and investigated, the previous tractography experience (intra‑ and interobserver massive presence of the fibers of each target tract reliability). was required. Therefore, the combination of multiple Table 1: Studies on tractography including intra‑ and interobserver agreement tests Authors Anatomic study Statistical analysis Variables Intraobserver Interobserver Catani et al.[3] No r FA, VOL, LEN, NTR No 10 observers vs. 1 observer Wakana et al.[27] No kappa, CV FA, PIXELS 1 observer 3 observers** Verhoeven et al.[29] No kappa PIXELS 3 observers 3 observers Danielian et al.[6] No ICC, kappa, CV MD, FA, AD, TD, PIXELS 2 observers 2 observers Ciccarelli et al.[5] No CV VOL, FA 1 observer 2 observers Malykhin et al.[20] No ICC, CV VOL, ADC, FA 1 observer 2 observers Bonekamp et al.[1] No ICC, CV ADC, FA 1 observer 4 observers This study Yes ICC, r FA, VOL, NTR, LEN, ADC, NVO 2 observers 2 observers* *Without previous experience with this method. ADC: Apparent diffusion coefficient; CV: Coefficient of variance; r: Pearson association coefficient; ICC: Intraclass correlation coefficients; FA: Fractional anisotropy; VOL: Volume; LEN: Length of tracts; NTR: Number of tracts; MD: Mean diffusivity; AD: Axial diffusivity; TD: Transverse diffusivity; NVO: Number of voxels Surgical Neurology International 2013, 4:51 http://www.surgicalneurologyint.com/content/4/1/51 ROIs with these fibers allowed improving anatomical Reconstruction protocol sensitivity and specificity at
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