Abstract
Purpose
Standard magnetic resonance imaging (MRI) does not depict the true extent of tumour cell invasion in gliomas. We investigated the feasibility of advanced imaging methods, i.e. diffusion tensor imaging (DTI), fibre tracking and O-(2-[18F]-fluoroethyl)-L-tyrosine (18F-FET) PET, for the detection of tumour invasion into white matter structures not visible in routine MRI.
Methods
DTI and fibre tracking was performed on ten patients with gliomas, WHO grades II-IV. Five patients experienced preoperative sensorimotor deficits. The ratio of fractional anisotropy (FA) between the ipsilateral and contralateral pyramidal tract was calculated. Twenty-one stereotactic biopsies from five patients were histopathologically evaluated for the absolute numbers and percentages of tumour cells. 18F-FET PET scans were performed and the bilateral ratio [ipsilateral-to-contralateral ratio (ICR)] of 18F-FET-uptake was calculated for both cross-sections of pyramidal tracts and biopsy sites.
Results
The FA ratio within the pyramidal tract was lower in patients with sensorimotor deficits (0.61–1.06) compared with the FA ratio in patients without sensorimotor deficits (0.92–1.06). In patients with preoperative sensorimotor deficits, we found a significantly (p = 0.028) higher ICR of 18F-FET uptake (1.01–1.59) than in patients without any deficits (0.96–1.08). The ICR of 18F-FET-uptake showed a strong correlation (r = 0.696, p = 0.001) with the absolute number of tumour cells and a moderate correlation (r = 0.535, p = 0.012) with the percentage of tumour cells.
Conclusions
Our data show an association between preoperative sensorimotor deficits, increased 18F-FET uptake and decreased FA ratio in the pyramidal tract. We demonstrated a correlation between tumour invasion and 18F-FET uptake. These findings may help to distinguish between edema versus tumour-associated neurological deficits and could prevent the destruction of important structures, like the pyramidal tract, during tumour operations by allowing more precise preoperative planning.
Similar content being viewed by others
References
Berman JI, Berger MS, Chung SW, Nagarajan SS, Henry RG (2007) Accuracy of diffusion tensor magnetic resonance imaging tractography assessed using intraoperative subcortical stimulation mapping and magnetic source imaging. J Neurosurg 107:488–494. doi:10.3171/JNS-07/09/0488
Berman JI, Berger MS, Mukherjee P, Henry RG (2004) Diffusion-tensor imaging-guided tracking of fibers of the pyramidal tract combined with intraoperative cortical stimulation mapping in patients with gliomas. J Neurosurg 101:66–72
Berman JI, Mukherjee P, Partridge SC, Miller SP, Ferriero DM, Barkovich AJ, Vigneron DB, Henry RG (2005) Quantitative diffusion tensor MRI fiber tractography of sensorimotor white matter development in premature infants. Neuroimage 27:862–871. doi:10.1016/j.neuroimage.2005.05.018
Cizek J, Herholz K, Vollmar S, Schrader R, Klein J, Heiss WD (2004) Fast and robust registration of PET and MR images of human brain. Neuroimage 22:434–442. doi:10.1016/j.neuroimage.2004.01.016
Clark CA, Barrick TR, Murphy MM, Bell BA (2003) White matter fiber tracking in patients with space-occupying lesions of the brain: a new technique for neurosurgical planning? Neuroimage 20:1601–1608. doi:10.1016/j.neuroimage.2003.07.022
Deichen JT, Prante O, Gack M, Schmiedehausen K, Kuwert T (2003) Uptake of [18F]fluorodeoxyglucose in human monocyte-macrophages in vitro. Eur J Nucl Med Mol Imaging 30:267–273
Floeth FW, Pauleit D, Sabel M, Reifenberger G, Stoffels G, Stummer W, Rommel F, Hamacher K, Langen KJ (2006) 18F-FET PET differentiation of ring-enhancing brain lesions. J Nucl Med 47:776–782
Floeth FW, Pauleit D, Sabel M, Stoffels G, Reifenberger G, Riemenschneider MJ, Jansen P, Coenen HH, Steiger HJ, Langen KJ (2007) Prognostic value of O-(2-[18F]-fluoroethyl)-L-tyrosine PET and MRI in low-grade glioma. J Nucl Med 48:519–527. doi:10.2967/jnumed.106.037895
Floeth FW, Sabel M, Stoffels G, Pauleit D, Hamacher K, Steiger HJ, Langen KJ (2008) Prognostic value of 18F-fluoroethyl-L-tyrosine PET and MRI in small nonspecific incidental brain lesions. J Nucl Med 49:730–737. doi:10.2967/jnumed.107.050005
Gruber S, Mlynarik V, Moser E (2003) High-resolution 3D proton spectroscopic imaging of the human brain at 3 T: SNR issues and application for anatomy-matched voxel sizes. Magn Reson Med 49:299–306. doi:10.1002/mrm.10377
Herzog H, Tellmann L, Hocke C, Pietrzyk U, Casey ME, Kuwert T (2004) NEMA NU2–2001 guided performance evaluation of four Siemens ECAT PET-Scanners. IEEE Trans Nucl Sci 51:2662–2669. doi:10.1109/TNS.2004.835778
Jiang H, van Zijl PC, Kim J, Pearlson GD, Mori S (2006) DtiStudio: resource program for diffusion tensor computation and fiber bundle tracking. Comput Methods Programs Biomed 81:106–116. doi:10.1016/j.cmpb.2005.08.004
Jones DK, Simmons A, Williams SC, Horsfield MA (1999) Non-invasive assessment of axonal fiber connectivity in the human brain via diffusion tensor MRI. Magn Reson Med 42:37–41. doi:10.1002/(SICI)1522-2594(199907)42:1<37::AID-MRM7>3.0.CO;2-O
Kaim AH, Weber B, Kurrer MO, Gottschalk J, Von Schulthess GK, Buck A (2002) Autoradiographic quantification of 18F-FDG uptake in experimental soft-tissue abscesses in rats. Radiology 223:446–451. doi:10.1148/radiol.2232010914
Kaim AH, Weber B, Kurrer MO, Westera G, Schweitzer A, Gottschalk J, von Schulthess GK, Buck A (2002) 18F-FDG and 18F-FET uptake in experimental soft tissue infection. Eur J Nucl Med Mol Imaging 29:648–654. doi:10.1007/s00259-002-0780-y
Kamada K, Todo T, Masutani Y, Aoki S, Ino K, Takano T, Kirino T, Kawahara N, Morita A (2005) Combined use of tractography-integrated functional neuronavigation and direct fiber stimulation. J Neurosurg 102:664–672
Kondziolka D, Lunsford LD, Martinez AJ (1993) Unreliability of contemporary neurodiagnostic imaging in evaluating suspected adult supratentorial (low-grade) astrocytoma. J Neurosurg 79:533–536
Kubota R, Yamada S, Kubota K, Ishiwata K, Tamahashi N, Ido T (1992) Intratumoral distribution of fluorine-18-fluorodeoxyglucose in vivo: high accumulation in macrophages and granulation tissues studied by microautoradiography. J Nucl Med 33:1972–1980
Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, Chabriat H (2001) Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 13:534–546. doi:10.1002/jmri.1076
Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:265–269. doi:10.1002/1531-8249(199902)45:2<265::AID-ANA21>3.0.CO;2-3
Mori S, Kaufmann WE, Davatzikos C, Stieltjes B, Amodei L, Fredericksen K, Pearlson GD, Melhem ER, Solaiyappan M, Raymond GV, Moser HW, van Zijl PC (2002) Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Magn Reson Med 47:215–223. doi:10.1002/mrm.10074
Nakaji H, Kouyama N, Muragaki Y, Kawakami Y, Iseki H (2008) Localization of nerve fiber bundles by polarization-sensitive optical coherence tomography. J Neurosci Methods 174:82–90. doi:10.1016/j.jneumeth.2008.07.004
Nimsky C, Ganslandt O, Hastreiter P, Wang R, Benner T, Sorensen AG, Fahlbusch R (2005) Intraoperative diffusion-tensor MR imaging: shifting of white matter tracts during neurosurgical procedures–initial experience. Radiology 234:218–225. doi:10.1148/radiol.2341031984
Pauleit D, Stoffels G, Schaden W, Hamacher K, Bauer D, Tellmann L, Herzog H, Broer S, Coenen HH, Langen KJ (2005) PET with O-(2-[18F]fluoroethyl)-L-tyrosine in peripheral tumors: First clinical results. J Nucl Med 46:411–416
Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36:893–906. doi:10.1002/mrm.1910360612
Pöpperl G, Goldbrunner R, Gildehaus FJ, Kreth FW, Tanner P, Holtmannspotter M, Tonn JC, Tatsch K (2005) O-(2-[18F]fluoroethyl)-L-tyrosine PET for monitoring the effects of convection-enhanced delivery of paclitaxel in patients with recurrent glioblastoma. Eur J Nucl Med Mol Imaging 32:1018–1025. doi:10.1007/s00259-005-1819-7
Pöpperl G, Gotz C, Rachinger W, Gildehaus FJ, Tonn JC, Tatsch K (2004) Value of O-(2-[18F]fluoroethyl)- L-tyrosine PET for the diagnosis of recurrent glioma. Eur J Nucl Med Mol Imaging 31:1464–1470. doi:10.1007/s00259-004-1590-1
Pöpperl G, Kreth FW, Herms J, Koch W, Mehrkens JH, Gildehaus FJ, Kretzschmar HA, Tonn JC, Tatsch K (2006) Analysis of 18F-FET PET for grading of recurrent gliomas: is evaluation of uptake kinetics superior to standard methods? J Nucl Med 47:393–403
Prante O, Blaser D, Maschauer S, Kuwert T (2007) In vitro characterization of the thyroidal uptake of O-(2-[18F]fluoroethyl)-L-tyrosine. Nucl Med Biol 34:305–314. doi:10.1016/j.nucmedbio.2006.12.007
Rachinger W, Goetz C, Pöpperl G, Gildehaus FJ, Kreth FW, Holtmannspotter M, Herms J, Koch W, Tatsch K, Tonn JC (2005) Positron emission tomography with O-(2-[18F]fluoroethyl)-L-tyrosine versus magnetic resonance imaging in the diagnosis of recurrent gliomas. Neurosurgery 57:505–511. doi:10.1227/01.NEU.0000171642.49553.B0
Rau FC, Weber WA, Wester HJ, Herz M, Becker I, Kruger A, Schwaiger M, Senekowitsch-Schmidtke R (2002) O-(2-[18F]Fluoroethyl)- L-tyrosine (FET): a tracer for differentiation of tumour from inflammation in murine lymph nodes. Eur J Nucl Med Mol Imaging 29:1039–1046. doi:10.1007/s00259-002-0821-6
Roberts TP, Liu F, Kassner A, Mori S, Guha A (2005) Fiber density index correlates with reduced fractional anisotropy in white matter of patients with glioblastoma. AJNR Am J Neuroradiol 26:2183–2186
Schonberg T, Pianka P, Hendler T, Pasternak O, Assaf Y (2006) Characterization of displaced white matter by brain tumors using combined DTI and fMRI. Neuroimage
Stadlbauer A, Ganslandt O, Buslei R, Hammen T, Gruber S, Moser E, Buchfelder M, Salomonowitz E, Nimsky C (2006) Gliomas: histopathologic evaluation of changes in directionality and magnitude of water diffusion at diffusion-tensor MR imaging. Radiology 240:803–810. doi:10.1148/radiol.2403050937
Stadlbauer A, Nimsky C, Buslei R, Salomonowitz E, Hammen T, Buchfelder M, Moser E, Ernst-Stecken A, Ganslandt O (2007) Diffusion tensor imaging and optimized fiber tracking in glioma patients: Histopathologic evaluation of tumor-invaded white matter structures. Neuroimage 34:949–956. doi:10.1016/j.neuroimage.2006.08.051
Stadlbauer A, Nimsky C, Gruber S, Moser E, Hammen T, Engelhorn T, Buchfelder M, Ganslandt O (2007) Changes in fiber integrity, diffusivity, and metabolism of the pyramidal tract adjacent to gliomas: a quantitative diffusion tensor fiber tracking and MR spectroscopic imaging study. AJNR Am J Neuroradiol 28:462–469
Stadlbauer A, Prante O, Nimsky C, Salomonowitz E, Buchfelder M, Kuwert T, Linke R, Ganslandt O (2008) Metabolic imaging of cerebral gliomas: spatial correlation of changes in O-(2–18F-fluoroethyl)-L-tyrosine PET and proton magnetic resonance spectroscopic imaging. J Nucl Med 49:721–729. doi:10.2967/jnumed.107.049213
Weckesser M, Langen KJ, Rickert CH, Kloska S, Straeter R, Hamacher K, Kurlemann G, Wassmann H, Coenen HH, Schober O (2005) O-(2-[18F]fluorethyl)-L-tyrosine PET in the clinical evaluation of primary brain tumours. Eur J Nucl Med Mol Imaging 32:422–429. doi:10.1007/s00259-004-1705-8
Wester HJ, Herz M, Weber W, Heiss P, Senekowitsch-Schmidtke R, Schwaiger M, Stocklin G (1999) Synthesis and radiopharmacology of O-(2-[18F]fluoroethyl)-L-tyrosine for tumor imaging. J Nucl Med 40:205–212
Yamada K, Kizu O, Mori S, Ito H, Nakamura H, Yuen S, Kubota T, Tanaka O, Akada W, Sasajima H, Mineura K, Nishimura T (2003) Brain fiber tracking with clinically feasible diffusion-tensor MR imaging: initial experience. Radiology 227:295–301. doi:10.1148/radiol.2271020313
Yu CS, Li KC, Xuan Y, Ji XM, Qin W (2005) Diffusion tensor tractography in patients with cerebral tumors: A helpful technique for neurosurgical planning and postoperative assessment. Eur J Radiol 56:197–204. doi:10.1016/j.ejrad.2005.04.010
Author information
Authors and Affiliations
Corresponding author
Additional information
Comments
The authors contribute a nice study which supports the growing information about the value of FET-PET to detect more precisely the true volume of a glioma. However, within a very small cohort of cases they mix low and high grade gliomas which of course had to be analyzed separately.
J.C. Tonn
Munich, Germany
Comment
This is a clear and well written article on the correlation of FET-PET and DTI tractography findings in the pyramidal tract in the presence or absence of symptoms of pyramidal tract involvement by grade II-IV gliomas. It is important that glioma surgeons extend intraoperative localization of eloquent areas from the cortex to the white matter tracts below. Identification of white matter tracts by electrical stimulation is most comprehensive in awake patients (1), but at least corticospinal connections can also be identified in anesthetized patients, in the absence of neuromuscular blocade, by EMG responses from face and limb muscles.
References
1. Duffau H, Peggy Gatignol ST, Mandonnet E, Capelle L, Taillandier L. Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere. J Neurosurg 2008;109:461–71.
Juha E Jaaskelainen
Kuopio, Finland
A. Stadlbauer and E. Pölking contributed equally to this study.
Rights and permissions
About this article
Cite this article
Stadlbauer, A., Pölking, E., Prante, O. et al. Detection of tumour invasion into the pyramidal tract in glioma patients with sensorimotor deficits by correlation of 18F-fluoroethyl-L-tyrosine PET and magnetic resonance diffusion tensor imaging. Acta Neurochir 151, 1061–1069 (2009). https://doi.org/10.1007/s00701-009-0378-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00701-009-0378-2