Diffusion tensor tractography of the arcuate fasciculus in patients with brain tumors: Comparison between deterministic and probabilistic models


Purpose: The purpose of this study was to compare the deterministic and probabilistic tracking methods of diffusion tensor white matter fiber tractography in patients with brain tumors. Materials and Methods: We identified 29 patients with left brain tumors <2 cmfrom the arcuate fasciculus who underwent pre-operative language fMRI and DTI. The arcuate fasciculus was reconstructed using a deterministic Fiber Assignment by Continuous Tracking (FACT) algorithm and a probabilistic method based on an extended Monte Carlo Random Walk algorithm. Tracking was controlled using two ROIs corresponding to Broca’s and Wernicke’s areas. Tracts in tumoraffected hemispheres were examined for extension between Broca’s and Wernicke’s areas, anterior-posterior length and volume, and compared with the normal contralateral tracts. Results: Probabilistic tracts displayed more complete anterior extension to Broca’s area than did FACT tracts on the tumor-affected and normal sides (p < 0.0001). The median length ratio for tumor: normal sides was greater for probabilistic tracts than FACT tracts (p < 0.0001). The median tract volume ratio for tumor: normal sides was also greater for probabilistic tracts than FACT tracts (p = 0.01). Conclusion: Probabilistic tractography reconstructs the arcuate fasciculus more completely and performs better through areas of tumor and/or edema. The FACT algorithm tends to underestimate the anterior-most fibers of the arcuate fasciculus, which are crossed by primary motor fibers.

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Li, Z. , Peck, K. , Brennan, N. , Jenabi, M. , Hsu, M. , Zhang, Z. , Holodny, A. and Young, R. (2013) Diffusion tensor tractography of the arcuate fasciculus in patients with brain tumors: Comparison between deterministic and probabilistic models. Journal of Biomedical Science and Engineering, 6, 192-200. doi: 10.4236/jbise.2013.62023.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Breier, J.I., Hasan, K.M., Zhang, W., Men, D. and Pa panicolaou, A.C. (2008) Language dysfunction after stroke and damage to white matter tracts evaluated using diffusion tensor imaging. American Journal of Neuroradiology, 29, 483-487. doi:10.3174/ajnr.A0846
[2] Marchina, S., Zhu, L.L., Norton, A., Zipse, L., Wan, C.Y. and Schlaug, G. (2011) Impairment of speech production predicted by lesion load of the left arcuate fasciculus. Stroke, 42, 2251-2256. doi:10.1161/STROKEAHA.110.606103
[3] Yamada, K., Nagakane, Y., Mizuno, T., Hosomi, A., Na kagawa, M. and Nishimura, T. (2007) MR tractography depicting damage to the arcuate fasciculus in a patient with conduction aphasia. Neurology, 68, 789. doi:10.1212/01.wnl.0000256348.65744.b2
[4] Whittle, I.R. and Fraser, D.E. (1991) Resolution of fluent dysphasia following excision of metastatic carcinoma from the arcuate fasciculus. British Journal of Neurosurgery, 5, 647-649. doi:10.3109/02688699109002891
[5] Catani, M., Jones, D.K. and Ffytche, D.H. (2005) Peri sylvian language networks of the human brain. Annals of Neurology, 57, 8-16. doi:10.1002/ana.20319
[6] Rilling, J.K., Glasser, M.F., Preuss, T.M., Ma, X., Zhao, T., Hu, X. and Behrens, T.E.J. (2008) The evolution of the arcuate fasciculus revealed with comparative DTI. Nature Neuroscience, 11, 426-428. doi:10.1038/nn2072
[7] Le Bihan, D., Breton, E., Lallemand, D., Grenier, P., Ca banis, E. and Laval-Jeantet, M. (1986) MR imaging of intravoxel incoherent motions: Application to diffusion and perfusion in neurologic disorders. Radiology, 161, 401-407.
[8] Basser, P.J., Mattiello, J. and LeBihan, D. (1994) MR dif fusion tensor spectroscopy and imaging. Biophysical Jour nal, 66, 259-267. doi:10.1016/S0006-3495(94)80775-1
[9] Moseley, M.E., Cohen, Y., Kucharczyk, J., Mintorovitch, J., Asgari, H.S., Wendland, M.F., Tsuruda, J. and Nor man, D. (1990) Diffusion-weighted MR imaging of anisotropic water diffusion in cat central nervous system. Radiology, 176, 439-445.
[10] Basser, P.J., Pajevic, S., Pierpaoli, C., Duda, J. and Al droubi, A. (2000) In vivo ?ber tractography using DT-MRI data. Magnetic Resonance in Medicine, 44, 625-632. doi:10.1002/1522-2594(200010)44:4<625::AID-MRM17>3.0.CO;2-O
[11] Shimony, J.S., Snyder, A.Z., Conturo, T.E. and Corbetta, M. (2004) The study of neural connectivity using diffusion tensor tracking. Cortex, 40, 213-215. doi:10.1016/S0010-9452(08)70955-9
[12] Mori, S., Crain, B.J., Chacko, V.P. and Van Zijl, P.C. (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Annals of Neurology, 45, 265-269. doi:10.1002/1531-8249(199902)45:2<265::AID-ANA21>3.0.CO;2-3
[13] Mori, S. and van Zijl, P.C.M. (2002) Fiber tracking: Prin ciples and strategies—A technical review. NMR in Bio medicine, 15, 468-480. doi:10.1002/nbm.781
[14] Behrens, T.E.J., Woolrich, M.W., Jenkinson, M., Johan sen-Berg, H., Nunes, R.G., Clare, S., Matthews, P.M., Brady, J.M. and Smith, S.M. (2003) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magnetic Resonance in Medicine, 50, 1077-1088. doi:10.1002/mrm.10609
[15] Hagmann, P., Thiran, J.-P., Jonasson, L., Vandergheynst, P., Clarke, S., Maeder, P. and Meuli, R. (2003) DTI map ping of human brain connectivity: Statistical fibre track ing and virtual dissection. Neuroimage, 19, 545-554. doi:10.1016/S1053-8119(03)00142-3
[16] Parker, G.J., Haroon, H.A. and Wheeler-Kingshott, C.A. (2003) A framework for a streamline-based probabilistic index of connectivity (PICo) using a structural interpretation of MRI diffusion measurements. Journal of Magnetic Resonance Imaging, 18, 242-254. doi:10.1002/jmri.10350
[17] Alexander, A.L., Hasan, K.M., Lazar, M., Tsuruda, J.S. and Parker, D.L. (2001) Analysis of partial volume effects in diffusion-tensor MRI. Magnetic Resonance in Medicine, 45, 770-780. doi:10.1002/mrm.1105
[18] Mori, S., Kaufmann, W.E., Davatzikos, C., et al. (2002) Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Magnetic Resonance in Medicine, 47, 215-223. doi:10.1002/mrm.10074
[19] Jellison, B.J., Field, A.S., Medow, J., Lazar, M., Shariar Salamat, M. and Alexander, A.L. (2004) Diffusion tensor imaging of cerebral white matter: A pictorial review of physics, fiber tract anatomy, and tumor imaging patterns. American Journal of Neurordiology, 25, 356-369.
[20] Kreher, B.W., Schnell, S., Mader, I., Il’yasov, K.A., Hen nig, J., Kiselev, V.G. and Saur, D. (2008) Connecting and merging fibres: Pathway extraction by combining probability maps. Neuroimage, 43, 81-89. doi:10.1016/j.neuroimage.2008.06.023
[21] Saur, D., Kreher, B.W., Schnell, S., Kummerer, D., Kell meyer, P., Vry, M.S., Umarova, R., Musso, M., Glauche, V., Abel, S., Huber, W., Rijntjes, M., Hennig, J. and Weiller, C. (2008) Ventral and dorsal pathways for language. Proceedings of the National Academy of Sciences of the USA, 105, 18035-18040. doi:10.1073/pnas.0805234105
[22] Catani, M., Jones, D.K. and Ffytche, D.H. (2005) Peri sylvian language networks of the human brain. Annals of Neurology, 57, 8-16. doi:10.1002/ana.20319
[23] Bernal, B. and Altman, N. (2010) The connectivity of the superior longitudinal fasciculus: A tractography DTI study. Magnetic Resonance Imaging, 28, 217-225. doi:10.1016/j.mri.2009.07.008
[24] Kreher, B., S S., Hennig, J. and Il’yasov, K. (2006) DTI calculation, fiber-tracking, and combined evaluation consolidated in a complete toolbox. Proceedings of the 12th Annual Meeting of the Organization for Human Brain Mapping, Florence,
[25] Kreher, B., Henning, J. and Il’yasov, K. (2006) DTI&Fiber-Tools: A complete toolbox for DTI calculation, fiber tracking, and combined evaluation. Proceeding of ISMRM 14th International Scientific Meeting, Seattle.
[26] Glasser, M.F. and Rilling, J. (2008) DTI tractography of the human brain’s language pathways. Cerebral Cortex, 18, 2471-2482. doi:10.1093/cercor/bhn011
[27] Ciccarelli, O., Behrens, T., Altmann, D.R., Orrell, R.W., Howard, R.S., Johansen-Berg, H., Miller, D.H., Matthews, P.M. and Thompson, A.J. (2006) Probabilistic diffusion tractography: A potential tool to assess the rate of disease progression in amyotrophic lateral sclerosis. Brain, 129, 1859-1871. doi:10.1093/brain/awl100
[28] Guye, M., Parker, G.J.M., Symms, M., Boulby, P., Wheeler Kingshott, C.A.M., Salek-Haddadi, A., Barker, G.J. and Duncan, J.S. (2003) Combined functional MRI and tractography to demonstrate the connectivity of the human primary motor cortex in vivo. Neuroimage, 19, 1349 1360. doi:10.1016/S1053-8119(03)00165-4
[29] Benjamini, Y. and Hochberg, Y. (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B (Methodological), 57, 289-300.
[30] Roux, F.E., Boulanouar, K., Ranjeva, J.P., Manelfe, C., Tremoulet, M., Sabatier, J. and Berry, I. (1999) Cortical intraoperative stimulation in brain tumors as a tool to evaluate spatial data from motor functional MRI. Investigative Radiology, 34, 225-229. doi:10.1097/00004424-199903000-00012
[31] Cosgrove, G.R., Buchbinder, B.R. and Jiang, H. (1996) Functional magnetic resonance imaging for intracranial navigation. Neurosurgery Clinics of North America, 7, 313 322.
[32] Mueller, W.M., Yetkin, F., Hammeke, T.A., Morris, G.L., Swanson, S.J., Reichert, K., Cox, R. and Haughton, V.M. (1996) Functional magnetic resonance imaging mapping of the motor cortex in patients with cerebral tumors. Neurosurgery, 39, 515-521.
[33] Geschwind, N. (1970) The organization of language and the brain. Science, 170, 940-944. doi:10.1126/science.170.3961.940
[34] Bernal, B. and Ardila, A. (2009) The role of the arcuate fasciculus in conduction aphasia. Brain, 132, 2309-2316. doi:10.1093/brain/awp206
[35] Mori, S. and van Zijil, P.C.M. (2002) Fiber tracking: Principles and strategies—A technical review. NMR Bio medicine, 15, 468-480. doi:10.1002/nbm.781
[36] Berman, J.I., B M., Mukherjee, P. and Henry, R.G. (2004) Diffusion-tensor imaging-guided tracking of fibers of the pyramidal tract combined with intraoperative cortical sti mulation mapping in patients with gliomas. Journal of Neurosurgery, 101, 66-72. doi:10.3171/jns.2004.101.1.0066
[37] Tuch, D.S., Reese, T.G., Wiegell, M.R and Wedeen, V.J. (2003) Diffusion MRI of complex neural architecture. Neuron, 40, 885-895. doi:10.1016/S0896-6273(03)00758-X
[38] Wedeen, V., R T., Tuch, D.S., Weigel, M.R., Dou, J.G., Weiskoff, R.M. and Chessler, D. (2000) Mapping fiber orientation spectra in cerebral white matter with fourier-transform diffusion MR [abstract]. Proceedings of the 8th Meeting of the International Society for Magnetic Resonance in Medicine, Berkeley, 82.
[39] Ciccarelli, O., Catani, M., Johansen-Berg, H., Clark, C. and Thompson, A. (2008) Diffusion-based tractography in neurological disorders: Concepts, applications, and future developments. The Lancet Neurology, 7, 715-727. doi:10.1016/S1474-4422(08)70163-7
[40] Fernandez-Miranda, J.C., Pathak, S. and Schneider, W. (2010) High-definition fiber tractography and language. Journal of Neurosurgery, 113, 156-157.
[41] Nimsky, C., Ganslandt, O., Merhof, D., Sorensen, A.G. and Fahlbusch, R. (2006) Intraoperative visualization of the pyramidal tract by diffusion tensor-imaging-based ?ber tracking. Neuroimage, 30, 1219-1229. doi:10.1016/j.neuroimage.2005.11.001
[42] Yu, C.S., Li, K.C., Xuan, Y., Ji, X.M. and Qin, W. (2005) Diffusion tensor tractography in patients with cerebral tumors: A helpful technique for neurosurgical planning and postoperative assessment. Radiology, 56, 197-204.
[43] Okada, T., Mikuni, N., Miki, Y., Kikuta, K., Urayama, S., Hanakawa, T., Fushimi, Y., Yamamoto, A., Kanagaki, M., Kukuyama, H., Hashimoto, N. and Togashi, K. (2006) Corticospinal tract localization: Integration of diffusion tensor tractography at 3-T MR Imaging with intraopera tive white matter stimulation mapping-preliminary results. Radiology, 240, 849-857. doi:10.1148/radiol.2403050916
[44] Nimsky, C., Ganslandt, O., Hastreiter, P., Wang, R., Ben ner, T., Sorensen, A.G. and Fahlbusch, R. (2005) Preoperative and intraoperative diffusion tensor imaging-based fiber tracking in glioma surgery. Neurosurgery, 56, 130 137.
[45] Berman, J.I., Berger, M., Chung, S.W., Nagarajan, S.S. and Henry, R.G. (2007) Accuracy of diffusion tensor magnetic resonance imaging tractography assessed using intraoperative subcortical stimulation mapping and mag netic source imaging. Journal of Neurosurgery, 107, 488 494. doi:10.3171/JNS-07/09/0488
[46] Kinoshita, M., Yamada, K., Hashimoto, N., Kato, A., Izumoto, S., Baba, T., Maruno, M., Nishimura, T. and Yoshimine, T. (2005) Fiber-tracking does not accurately estimate size of fiber bundle in pathological condition: Ini tial neurosurgical experience using neuronavigation and subcortical white matter stimulation. Neuroimage, 25, 424 429. doi:10.1016/j.neuroimage.2004.07.076
[47] Parker, G.J., Luzzi, S., Alexander, D.C., Wheeler-King shott, C.A., Ciccarelli, O. and Lambon Ralph, M.A. (2005) Lateralization of ventral and dorsal auditory-language pathways in the human brain. Neuroimage, 24, 656-666. doi:10.1016/j.neuroimage.2004.08.047
[48] Nucifora, P.G.P., Verma, R. and Melhem, E.R. (2005) Leftward asymmetry in relative fiber density of the arcuate fasciculus. Neuroreport, 16, 791-794. doi:10.1097/00001756-200505310-00002
[49] Chapman, C.H., Nagesh, V., Sundgren, P.C., et al. (2012) Diffusion tensor imaging of normal-appearing white matter as biomarker for radiation-induced late delayed cogni tive decline. International Journal of Radiation Oncology, Biology and Physics, 82, 2033-2040. doi:10.1016/j.ijrobp.2011.01.068
[50] Welzel, T., Niethammer, A., Mende, U., et al. (2008) Dif fusion tensor imaging screening of radiation-induced changes in the white matter after prophylactic cranial irradiation of patients with small cell lung cancer: First results of a prospective study. American Journal of Neuro radiology, 29, 379-383. doi:10.3174/ajnr.A0797
[51] Mabbott, D.J., Noseworthy, M.D., Bouffet, E., Rockel, C. and Laughlin, S. (2006) Diffusion tensor imaging of white matter after cranial radiation in children for medulloblastoma: Correlation with IQ. Neuro-Oncology, 8, 244-252. doi:10.1215/15228517-2006-002
[52] Abraham, J., Haut, M.W., Moran, M.T., Filburn, S., Le miuex, S. and Kuwabara, H. (2008) Adjuvant chemo therapy for breast cancer: effects on cerebral white matter seen in diffusion tensor imaging. Clinical Breast Cancer, 8, 88-91. doi:10.3816/CBC.2008.n.007
[53] Sijens, P.E., Heesters, M.A., Enting, R.H., et al. (2007) Diffusion tensor imaging and chemical shift imaging assessment of heterogeneity in low grade glioma under te mozolomide chemotherapy. Cancer Investigation, 25, 706 710. doi:10.1080/07357900701564028
[54] Matsukado, Y., MacCarty, C.S. and Kernohan, J.W. (1961) The growth of glioblastoma multiforme (astrocytomas, grades 3 and 4) in neurosurgical practice. Journal of Neurosurgery, 18, 636-644. doi:10.3171/jns.1961.18.5.0636
[55] Johnson, P.C., Hunt, S.J. and Drayer, B.P. (1989) Human cerebral gliomas: Correlation of postmortem MR imaging and neuropathologic findings. Radiology, 170, 211-217.
[56] Price, S.J., Burnet, N.G., Donovan, T., Green, H.A., Pena, A., Antoun, N.M., Pickard, J.D., Carpenter, T.A. and Gil lard, J.H. (2003) Diffusion tensor imaging of brain tumours at 3T: A potential tool for assessing white matter tract invasion? Clinical Radiology, 58, 455-462. doi:10.1016/S0009-9260(03)00115-6
[57] Kleihues, P. and Cavenee, W.K. (2000) Pathology and genetics of tumours of the nervous system. IARC Press, Lyon.
[58] Wieshmann, U.C., Symms, M., Parker, G.J.M., Clark, C., Lemieux, L., Barker, G. and Shorvon, S. (2000) Diffusion tensor imaging demonstrates deviation of fibres in normal appearing white matter adjacent to a brain tumour. Journal of Neurology, Neurosurgery & Psychiatry, 68, 501 503. doi:10.1136/jnnp.68.4.501

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