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Published in: Neuroradiology 1/2010

01-01-2010 | Functional Neuroradiology

Impact of fMRI-guided advanced DTI fiber tracking techniques on their clinical applications in patients with brain tumors

Authors: Raimund Kleiser, Philipp Staempfli, Anton Valavanis, Peter Boesiger, Spyros Kollias

Published in: Neuroradiology | Issue 1/2010

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Abstract

Introduction

White matter tractography based on diffusion tensor imaging has become a well-accepted non-invasive tool for exploring the white matter architecture of the human brain in vivo. There exist two main key obstacles for reconstructing white matter fibers: firstly, the implementation and application of a suitable tracking algorithm, which is capable of reconstructing anatomically complex fascicular pathways correctly, as, e.g., areas of fiber crossing or branching; secondly, the definition of an appropriate tracking seed area for starting the reconstruction process. Large intersubject, anatomical variations make it difficult to define tracking seed areas based on reliable anatomical landmarks. An accurate definition of seed regions for the reconstruction of a specific neuronal pathway becomes even more challenging in patients suffering from space occupying pathological processes as, e.g., tumors due to the displacement of the tissue and the distortion of anatomical landmarks around the lesion.

Methods

To resolve the first problem, an advanced tracking algorithm, called advanced fast marching, was applied in this study. The second challenge was overcome by combining functional magnetic resonance imaging (fMRI) and diffusion tensor imaging (DTI) in order to perform fMRI-guided accurate definition of appropriate seed areas for the DTI fiber tracking. In addition, the performance of the tasks was controlled by a MR-compatible power device.

Results

Application of this combined approach to eight healthy volunteers and exemplary to three tumor patients showed that it is feasible to accurately reconstruct relevant fiber tracts belonging to a specific functional system.

Conclusion

fMRI-guided advanced DTI fiber tracking has the potential to provide accurate anatomical and functional information for a more informed therapeutic decision making.
Literature
1.
go back to reference Arfanakis K, Gui M, Lazar M (2006) Optimization of white matter tractography for pre-surgical planning and image-guided surgery. Oncol Rep 15:1061–1064PubMed Arfanakis K, Gui M, Lazar M (2006) Optimization of white matter tractography for pre-surgical planning and image-guided surgery. Oncol Rep 15:1061–1064PubMed
2.
go back to reference Bammer R, Auer M, Keeling SL, Augustin M, Stables LA, Prokesch RW, Stollberger R, Moseley ME, Fazekas F (2002) Diffusion tensor imaging using single-shot SENSE-EPI. Magn Reson Med 48:128–136. doi:10.1002/mrm.10184 CrossRefPubMed Bammer R, Auer M, Keeling SL, Augustin M, Stables LA, Prokesch RW, Stollberger R, Moseley ME, Fazekas F (2002) Diffusion tensor imaging using single-shot SENSE-EPI. Magn Reson Med 48:128–136. doi:10.​1002/​mrm.​10184 CrossRefPubMed
7.
go back to reference Beisteiner R, Lanzenberger R, Novak K, Edward V, Windischberger C, Erdler M, Cunnington R, Gartus A, Streibl B, Moser E, Czech T, Deecke L (2000) Improvement of presurgical patient evaluation by generation of functional magnetic resonance risk maps. Neurosci Lett 290:13–16. doi:10.1016/S0304-3940(00)01303-3 CrossRefPubMed Beisteiner R, Lanzenberger R, Novak K, Edward V, Windischberger C, Erdler M, Cunnington R, Gartus A, Streibl B, Moser E, Czech T, Deecke L (2000) Improvement of presurgical patient evaluation by generation of functional magnetic resonance risk maps. Neurosci Lett 290:13–16. doi:10.​1016/​S0304-3940(00)01303-3 CrossRefPubMed
8.
go back to reference Filippi M, Cercignani M, Inglese M, Horsfield MA, Comi G (2001) Diffusion tensor magnetic resonance imaging in multiple sclerosis. Neurology 56:304–311PubMed Filippi M, Cercignani M, Inglese M, Horsfield MA, Comi G (2001) Diffusion tensor magnetic resonance imaging in multiple sclerosis. Neurology 56:304–311PubMed
9.
go back to reference Frackowiak RSJ, Friston KJ, Frith C (2004) Human brain function. Academic, New York Frackowiak RSJ, Friston KJ, Frith C (2004) Human brain function. Academic, New York
11.
go back to reference Goebell E, Fiehler J, Ding XQ, Paustenbach S, Nietz S, Heese O, Kucinski T, Hagel C, Westphal M, Zeumer H (2006) Disarrangement of fiber tracts and decline of neuronal density correlate in glioma patients—a combined diffusion tensor imaging and 1H-MR spectroscopy study. AJNR Am J Neuroradiol 27:1426–1431PubMed Goebell E, Fiehler J, Ding XQ, Paustenbach S, Nietz S, Heese O, Kucinski T, Hagel C, Westphal M, Zeumer H (2006) Disarrangement of fiber tracts and decline of neuronal density correlate in glioma patients—a combined diffusion tensor imaging and 1H-MR spectroscopy study. AJNR Am J Neuroradiol 27:1426–1431PubMed
12.
go back to reference Goebell E, Paustenbach S, Vaeterlein O, Ding XQ, Heese O, Fiehler J, Kucinski T, Hagel C, Westphal M, Zeumer H (2006) Low-grade and anaplastic gliomas: differences in architecture evaluated with diffusion-tensor MR imaging. Radiology 239:217–222. doi:10.1148/radiol.2383050059 CrossRefPubMed Goebell E, Paustenbach S, Vaeterlein O, Ding XQ, Heese O, Fiehler J, Kucinski T, Hagel C, Westphal M, Zeumer H (2006) Low-grade and anaplastic gliomas: differences in architecture evaluated with diffusion-tensor MR imaging. Radiology 239:217–222. doi:10.​1148/​radiol.​2383050059 CrossRefPubMed
13.
go back to reference Guye M, Parker GJ, Symms M, Boulby P, Wheeler-Kingshott CA, Salek-Haddadi A, Barker GJ, Duncan JS (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 CrossRefPubMed Guye M, Parker GJ, Symms M, Boulby P, Wheeler-Kingshott CA, Salek-Haddadi A, Barker GJ, Duncan JS (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 CrossRefPubMed
14.
go back to reference Helton KJ, Phillips NS, Khan RB, Boop FA, Sanford RA, Zou P, Li CS, Langston JW, Ogg RJ (2006) Diffusion tensor imaging of tract involvement in children with pontine tumors. AJNR Am J Neuroradiol 27:786–793PubMed Helton KJ, Phillips NS, Khan RB, Boop FA, Sanford RA, Zou P, Li CS, Langston JW, Ogg RJ (2006) Diffusion tensor imaging of tract involvement in children with pontine tumors. AJNR Am J Neuroradiol 27:786–793PubMed
16.
go back to reference Jaermann T, Crelier G, Pruessmann KP, Golay X, Netsch T, van Muiswinkel AM, Mori S, van Zijl PC, Valavanis A, Kollias S, Boesiger P (2004) SENSE-DTI at 3 T. Magn Reson Med 51:230–236. doi:10.1002/mrm.10707 CrossRefPubMed Jaermann T, Crelier G, Pruessmann KP, Golay X, Netsch T, van Muiswinkel AM, Mori S, van Zijl PC, Valavanis A, Kollias S, Boesiger P (2004) SENSE-DTI at 3 T. Magn Reson Med 51:230–236. doi:10.​1002/​mrm.​10707 CrossRefPubMed
19.
go back to reference Karonen JO, Liu Y, Vanninen RL, Ostergaard L, Kaarina Partanen PL, Vainio PA, Vanninen EJ, Nuutinen J, Roivainen R, Soimakallio S, Kuikka JT, Aronen HJ (2000) Combined perfusion- and diffusion-weighted MR imaging in acute ischemic stroke during the 1st week: a longitudinal study. Radiology 217:886–894PubMed Karonen JO, Liu Y, Vanninen RL, Ostergaard L, Kaarina Partanen PL, Vainio PA, Vanninen EJ, Nuutinen J, Roivainen R, Soimakallio S, Kuikka JT, Aronen HJ (2000) Combined perfusion- and diffusion-weighted MR imaging in acute ischemic stroke during the 1st week: a longitudinal study. Radiology 217:886–894PubMed
20.
go back to reference Karonen JO, Vanninen RL, Liu Y, Ostergaard L, Kuikka JT, Nuutinen J, Vanninen EJ, Partanen PL, Vainio PA, Korhonen K, Perkio J, Roivainen R, Sivenius J, Aronen HJ (1999) Combined diffusion and perfusion MRI with correlation to single-photon emission CT in acute ischemic stroke. Ischemic penumbra predicts infarct growth. Stroke 30:1583–1590PubMed Karonen JO, Vanninen RL, Liu Y, Ostergaard L, Kuikka JT, Nuutinen J, Vanninen EJ, Partanen PL, Vainio PA, Korhonen K, Perkio J, Roivainen R, Sivenius J, Aronen HJ (1999) Combined diffusion and perfusion MRI with correlation to single-photon emission CT in acute ischemic stroke. Ischemic penumbra predicts infarct growth. Stroke 30:1583–1590PubMed
23.
go back to reference Lazar M, Alexander AL, Thottakara PJ, Badie B, Field AS (2006) White matter reorganization after surgical resection of brain tumors and vascular malformations. AJNR Am J Neuroradiol 27:1258–1271PubMed Lazar M, Alexander AL, Thottakara PJ, Badie B, Field AS (2006) White matter reorganization after surgical resection of brain tumors and vascular malformations. AJNR Am J Neuroradiol 27:1258–1271PubMed
24.
go back to reference Lazar M, Weinstein DM, Tsuruda JS, Hasan KM, Arfanakis K, Meyerand ME, Badie B, Rowley HA, Haughton V, Field A, Alexander AL (2003) White matter tractography using diffusion tensor deflection. Hum Brain Mapp 18:306–321. doi:10.1002/hbm.10102 CrossRefPubMed Lazar M, Weinstein DM, Tsuruda JS, Hasan KM, Arfanakis K, Meyerand ME, Badie B, Rowley HA, Haughton V, Field A, Alexander AL (2003) White matter tractography using diffusion tensor deflection. Hum Brain Mapp 18:306–321. doi:10.​1002/​hbm.​10102 CrossRefPubMed
29.
go back to reference Nimsky C, Ganslandt O, Hastreiter P, Wang R, Benner T, Sorensen AG, Fahlbusch R (2005) Preoperative and intraoperative diffusion tensor imaging-based fiber tracking in glioma surgery. Neurosurgery 56:130–137 discussion 138PubMed Nimsky C, Ganslandt O, Hastreiter P, Wang R, Benner T, Sorensen AG, Fahlbusch R (2005) Preoperative and intraoperative diffusion tensor imaging-based fiber tracking in glioma surgery. Neurosurgery 56:130–137 discussion 138PubMed
31.
go back to reference Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G (1996) Diffusion tensor MR imaging of the human brain. Radiology 201:637–648PubMed Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G (1996) Diffusion tensor MR imaging of the human brain. Radiology 201:637–648PubMed
33.
go back to reference Rovaris M, Bozzali M, Iannucci G, Ghezzi A, Caputo D, Montanari E, Bertolotto A, Bergamaschi R, Capra R, Mancardi GL, Martinelli V, Comi G, Filippi M (2002) Assessment of normal-appearing white and gray matter in patients with primary progressive multiple sclerosis: a diffusion-tensor magnetic resonance imaging study. Arch Neurol 59:1406–1412. doi:10.1001/archneur.59.9.1406 CrossRefPubMed Rovaris M, Bozzali M, Iannucci G, Ghezzi A, Caputo D, Montanari E, Bertolotto A, Bergamaschi R, Capra R, Mancardi GL, Martinelli V, Comi G, Filippi M (2002) Assessment of normal-appearing white and gray matter in patients with primary progressive multiple sclerosis: a diffusion-tensor magnetic resonance imaging study. Arch Neurol 59:1406–1412. doi:10.​1001/​archneur.​59.​9.​1406 CrossRefPubMed
34.
go back to reference Rovaris M, Gallo A, Valsasina P, Benedetti B, Caputo D, Ghezzi A, Montanari E, Sormani MP, Bertolotto A, Mancardi G, Bergamaschi R, Martinelli V, Comi G, Filippi M (2005) Short-term accrual of gray matter pathology in patients with progressive multiple sclerosis: an in vivo study using diffusion tensor MRI. Neuroimage 24:1139–1146. doi:10.1016/j.neuroimage.2004.10.006 CrossRefPubMed Rovaris M, Gallo A, Valsasina P, Benedetti B, Caputo D, Ghezzi A, Montanari E, Sormani MP, Bertolotto A, Mancardi G, Bergamaschi R, Martinelli V, Comi G, Filippi M (2005) Short-term accrual of gray matter pathology in patients with progressive multiple sclerosis: an in vivo study using diffusion tensor MRI. Neuroimage 24:1139–1146. doi:10.​1016/​j.​neuroimage.​2004.​10.​006 CrossRefPubMed
36.
go back to reference Schwamm LH, Koroshetz WJ, Sorensen AG, Wang B, Copen WA, Budzik R, Rordorf G, Buonanno FS, Schaefer PW, Gonzalez RG (1998) Time course of lesion development in patients with acute stroke: serial diffusion- and hemodynamic-weighted magnetic resonance imaging. Stroke 29:2268–2276PubMed Schwamm LH, Koroshetz WJ, Sorensen AG, Wang B, Copen WA, Budzik R, Rordorf G, Buonanno FS, Schaefer PW, Gonzalez RG (1998) Time course of lesion development in patients with acute stroke: serial diffusion- and hemodynamic-weighted magnetic resonance imaging. Stroke 29:2268–2276PubMed
37.
go back to reference Smits M, Vernooij MW, Wielopolski PA, Vincent AJ, Houston GC, van der Lugt A (2007) Incorporating functional MR imaging into diffusion tensor tractography in the preoperative assessment of the corticospinal tract in patients with brain tumors. AJNR Am J Neuroradiol 28:1354–1361. doi:10.3174/ajnr.A0538 CrossRefPubMed Smits M, Vernooij MW, Wielopolski PA, Vincent AJ, Houston GC, van der Lugt A (2007) Incorporating functional MR imaging into diffusion tensor tractography in the preoperative assessment of the corticospinal tract in patients with brain tumors. AJNR Am J Neuroradiol 28:1354–1361. doi:10.​3174/​ajnr.​A0538 CrossRefPubMed
39.
go back to reference Staempfli P, Jaermann T, Valavanis A, Boesiger P, Kollias S (2004) fMRI based fiber tracking using SENSE-DTI at 3 Tesla. Presented at Proc Intl Soc Magn Reson Med, Kyoto, Japan, 2004. Staempfli P, Jaermann T, Valavanis A, Boesiger P, Kollias S (2004) fMRI based fiber tracking using SENSE-DTI at 3 Tesla. Presented at Proc Intl Soc Magn Reson Med, Kyoto, Japan, 2004.
40.
41.
go back to reference Staempfli P, Rienmueller A, Reischauer C, Valavanis A, Boesiger P, Kollias S (2007) Reconstruction of the human visual system based on DTI fiber tracking. J Magn Reson Imaging 26:886–893. doi:10.1002/jmri.21098 CrossRefPubMed Staempfli P, Rienmueller A, Reischauer C, Valavanis A, Boesiger P, Kollias S (2007) Reconstruction of the human visual system based on DTI fiber tracking. J Magn Reson Imaging 26:886–893. doi:10.​1002/​jmri.​21098 CrossRefPubMed
42.
go back to reference Tournier JD, Calamante F, King MD, Gadian DG, Connelly A (2002) Limitations and requirements of diffusion tensor fiber tracking: an assessment using simulations. Magn Reson Med 47:701–708. doi:10.1002/mrm.10116 CrossRefPubMed Tournier JD, Calamante F, King MD, Gadian DG, Connelly A (2002) Limitations and requirements of diffusion tensor fiber tracking: an assessment using simulations. Magn Reson Med 47:701–708. doi:10.​1002/​mrm.​10116 CrossRefPubMed
43.
go back to reference Upadhyay J, Ducros M, Knaus TA, Lindgren KA, Silver A, Tager-Flusberg H, Kim DS (2007) Function and connectivity in human primary auditory cortex: a combined fMRI and DTI study at 3 Tesla. Cereb Cortex 17:2420–2432. doi:10.1093/cercor/bhl150 CrossRefPubMed Upadhyay J, Ducros M, Knaus TA, Lindgren KA, Silver A, Tager-Flusberg H, Kim DS (2007) Function and connectivity in human primary auditory cortex: a combined fMRI and DTI study at 3 Tesla. Cereb Cortex 17:2420–2432. doi:10.​1093/​cercor/​bhl150 CrossRefPubMed
45.
go back to reference Watts R, Liston C, Niogi S, Ulug AM (2003) Fiber tracking using magnetic resonance diffusion tensor imaging and its applications to human brain development. Ment Retard Dev Disabil Res Rev 9:168–177. doi:10.1002/mrdd.10077 CrossRefPubMed Watts R, Liston C, Niogi S, Ulug AM (2003) Fiber tracking using magnetic resonance diffusion tensor imaging and its applications to human brain development. Ment Retard Dev Disabil Res Rev 9:168–177. doi:10.​1002/​mrdd.​10077 CrossRefPubMed
46.
go back to reference Weinstein D, Kindlmann G, Lundberg E (1999) Tensorlines: advection-diffusion based propagation through diffusion tensor fields. IEEE Visualisation:249–253. Weinstein D, Kindlmann G, Lundberg E (1999) Tensorlines: advection-diffusion based propagation through diffusion tensor fields. IEEE Visualisation:249–253.
48.
go back to reference Witwer BP, Moftakhar R, Hasan KM, Deshmukh P, Haughton V, Field A, Arfanakis K, Noyes J, Moritz CH, Meyerand ME, Rowley HA, Alexander AL, Badie B (2002) Diffusion-tensor imaging of white matter tracts in patients with cerebral neoplasm. J Neurosurg 97:568–575CrossRefPubMed Witwer BP, Moftakhar R, Hasan KM, Deshmukh P, Haughton V, Field A, Arfanakis K, Noyes J, Moritz CH, Meyerand ME, Rowley HA, Alexander AL, Badie B (2002) Diffusion-tensor imaging of white matter tracts in patients with cerebral neoplasm. J Neurosurg 97:568–575CrossRefPubMed
49.
go back to reference Yasargil MG (1994) CNS tumors. Thieme Medical, New York Yasargil MG (1994) CNS tumors. Thieme Medical, New York
51.
go back to reference Zhang S, Bastin ME, Laidlaw DH, Sinha S, Armitage PA, Deisboeck TS (2004) Visualization and analysis of white matter structural asymmetry in diffusion tensor MRI data. Magn Reson Med 51:140–147. doi:10.1002/mrm.10673 CrossRefPubMed Zhang S, Bastin ME, Laidlaw DH, Sinha S, Armitage PA, Deisboeck TS (2004) Visualization and analysis of white matter structural asymmetry in diffusion tensor MRI data. Magn Reson Med 51:140–147. doi:10.​1002/​mrm.​10673 CrossRefPubMed
Metadata
Title
Impact of fMRI-guided advanced DTI fiber tracking techniques on their clinical applications in patients with brain tumors
Authors
Raimund Kleiser
Philipp Staempfli
Anton Valavanis
Peter Boesiger
Spyros Kollias
Publication date
01-01-2010
Publisher
Springer-Verlag
Published in
Neuroradiology / Issue 1/2010
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI
https://doi.org/10.1007/s00234-009-0539-2

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