, Volume 60, Issue 3, pp 267–280 | Cite as

Generalized q-sampling imaging fiber tractography reveals displacement and infiltration of fiber tracts in low-grade gliomas

  • Pinar Celtikci
  • David T. Fernandes-Cabral
  • Fang-Cheng Yeh
  • Sandip S. Panesar
  • Juan C. Fernandez-MirandaEmail author
Diagnostic Neuroradiology



Low-grade gliomas (LGGs) are slow growing brain tumors that often cause displacement and/or infiltration of the surrounding white matter pathways. Differentiation between infiltration and displacement of fiber tracts remains a challenge. Currently, there is no reliable noninvasive imaging method capable of revealing such white matter alteration patterns. We employed quantitative anisotropy (QA) derived from generalized q-sampling imaging (GQI) to identify patterns of fiber tract alterations by LGGs.


Sixteen patients with a neuropathological diagnosis of LGG (WHO grade II) were enrolled. Peritumoral fiber tracts underwent qualitative and quantitative evaluation. Contralateral hemisphere counterparts were used for comparison. Tracts were qualitatively classified as unaffected, displaced, infiltrated or displaced, and infiltrated at once. The average QA of whole tract (W), peritumoral tract segment (S), and their ratio (S/W) were obtained and compared to the healthy side for quantitative evaluation.


Qualitative analysis revealed 9 (13.8%) unaffected, 24 (36.9%) displaced, 13 (20%) infiltrated, and 19 (29.2%) tracts with a combination of displacement and infiltration. There were no disrupted tracts. There was a significant increase in S/W ratio among displaced tracts in the pre-operative scans in comparison with the contralateral side. QA values of peritumoral tract segments (S) were significantly lower in infiltrated tracts.


WHO grade II LGGs might displace, infiltrate, or cause a combination of displacement and infiltration of WM tracts. QA derived from GQI provides valuable information that helps to differentiate infiltration from displacement. Anisotropy changes correlate with qualitative alterations, which may serve as a potential biomarker of fiber tract integrity.


Diffusion magnetic resonance imaging Fiber tractography Low-grade glioma Quantitative anisotropy White matter 



The authors would like to acknowledge the contribution of Yue-Fang Chang, Ph.D., in providing statistical analyses.

Compliance with ethical standards


This research was funded by a Seed Grant from the University of Pittsburgh Brain Institute and was partly funded by the Walter L. Copeland Fund of the Pittsburgh Foundation for Cranial Research.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards. For this type of study formal consent is not required.

Informed consent

For this type of retrospective study formal consent is not required.

Supplementary material

234_2018_1985_MOESM1_ESM.docx (39 kb)
ESM 1 (DOCX 38 kb)


  1. 1.
    Sanai N, Chang S, Berger MS (2011) Low-grade gliomas in adults. J Neurosurg 115(5):948–965. CrossRefPubMedGoogle Scholar
  2. 2.
    Grier JT, Batchelor T (2006) Low-grade gliomas in adults. Oncologist 11(6):681–693. CrossRefPubMedGoogle Scholar
  3. 3.
    Duffau H (2006) New concepts in surgery of WHO grade II gliomas: functional brain mapping, connectionism and plasticity—a review. J Neuro-Oncol 79(1):77–115. CrossRefGoogle Scholar
  4. 4.
    Wessels PH, Weber WEJ, Raven G, Ramaekers FCS, Hopman AHN, Twijnstra A (2003) Supratentorial grade II astrocytoma: biological features and clinical course. Lancet Neurol 2(7):395–403. CrossRefPubMedGoogle Scholar
  5. 5.
    Berger MS, Deliganis AV, Dobbins J, Keles GE (1994) The effect of extent of resection on recurrence in patients with low grade cerebral hemisphere gliomas. Cancer 74(6):1784–1791.<1784::AID-CNCR2820740622>3.0.CO;2-D CrossRefPubMedGoogle Scholar
  6. 6.
    Nakamura M, Konishi N, Tsunoda S, Nakase H, Tsuzuki T, Aoki H, Sakitani H, Inui T, Sakaki T (2000) Analysis of prognostic and survival factors related to treatment of low-grade astrocytomas in adults. Oncology 58(2):108–116CrossRefPubMedGoogle Scholar
  7. 7.
    Gousias K, Schramm J, Simon M (2014) Extent of resection and survival in supratentorial infiltrative low-grade gliomas: analysis of and adjustment for treatment bias. Acta Neurochir 156(2):327–337. CrossRefPubMedGoogle Scholar
  8. 8.
    Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, Tihan T, VandenBerg S, McDermott MW, Berger MS (2008) Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 26(8):1338–1345. CrossRefPubMedGoogle Scholar
  9. 9.
    Ius T, Isola M, Budai R et al (2012) Low-grade glioma surgery in eloquent areas: volumetric analysis of extent of resection and its impact on overall survival. A single-institution experience in 190 patients: clinical article. J Neurosurg 117(6):1039–1052. CrossRefPubMedGoogle Scholar
  10. 10.
    Fernandez-Miranda JC, Pathak S, Engh J et al (2012) High-definition fiber tractography of the human brain: neuroanatomical validation and neurosurgical applications. Neurosurgery 71(2):430–453. CrossRefPubMedGoogle Scholar
  11. 11.
    Basser PJ, Mattiello J, LeBihan D (1994) MR diffusion tensor spectroscopy and imaging. Biophys J 66(1):259–267. CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Field AS, Alexander AL, Wu Y-C, Hasan KM, Witwer B, Badie B (2004) Diffusion tensor eigenvector directional color imaging patterns in the evaluation of cerebral white matter tracts altered by tumor. J Magn Reson Imaging 20(4):555–562. CrossRefPubMedGoogle Scholar
  13. 13.
    Jellison BJ, Field AS, Medow J, Lazar M, Salamat MS, Alexander AL (2004) Diffusion tensor imaging of cerebral white matter: a pictorial review of physics, fiber tract anatomy, and tumor imaging patterns. AJNR Am J Neuroradiol 25(3):356–369PubMedGoogle Scholar
  14. 14.
    Alexander AL, Hasan KM, Lazar M, Tsuruda JS, Parker DL (2001) Analysis of partial volume effects in diffusion-tensor MRI. Magn Reson Med 45(5):770–780. CrossRefPubMedGoogle Scholar
  15. 15.
    Le Bihan D, Poupon C, Amadon A, Lethimonnier F (2006) Artifacts and pitfalls in diffusion MRI. J Magn Reson Imaging 24(3):478–488. CrossRefPubMedGoogle Scholar
  16. 16.
    Chung H-W, Chou M-C, Chen C-Y (2011) Principles and limitations of computational algorithms in clinical diffusion tensor MR tractography. AJNR Am J Neuroradiol 32:3–13. CrossRefPubMedGoogle Scholar
  17. 17.
    Jeurissen B, Leemans A, Tournier J-D et al (2013) Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging. Hum Brain Mapp 34(11):2747–2766. CrossRefPubMedGoogle Scholar
  18. 18.
    Jbabdi S, Behrens TEJ, Smith SM (2010) Crossing fibres in tract-based spatial statistics. Neuro Image 49(1):249–256. PubMedGoogle Scholar
  19. 19.
    Vos SB, Jones DK, Jeurissen B, Viergever MA, Leemans A (2012) The influence of complex white matter architecture on the mean diffusivity in diffusion tensor MRI of the human brain. Neuro Image 59(3):2208–2216. PubMedGoogle Scholar
  20. 20.
    Witwer BP, Moftakhar R, Hasan KM et al (2002) Diffusion-tensor imaging of white matter tracts in patients with cerebral neoplasm. J Neurosurg 97(3):568–575. CrossRefPubMedGoogle Scholar
  21. 21.
    Price SJ, Peña A, Burnet NG et al (2004) Tissue signature characterisation of diffusion tensor abnormalities in cerebral gliomas. Eur Radiol 14(10):1909–1917. CrossRefPubMedGoogle Scholar
  22. 22.
    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(2):197–204. CrossRefPubMedGoogle Scholar
  23. 23.
    Goebell E, Paustenbach S, Vaeterlein O et al (2006) Low-grade and anaplastic gliomas: differences in architecture evaluated with diffusion-tensor MR imaging. Radiology 239(1):217–222. CrossRefPubMedGoogle Scholar
  24. 24.
    Talos I-F, Zou KH, Kikinis R, Jolesz FA (2007) Volumetric assessment of tumor infiltration of adjacent white matter based on anatomic MRI and diffusion tensor tractography. Acad Radiol 14(4):431–436. CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Campanella M, Ius T, Skrap M, Fadiga L (2014) Alterations in fiber pathways reveal brain tumor typology: a diffusion tractography study. Peer J 2:e497. CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Delgado AF, Nilsson M, Latini F, Mårtensson J, Zetterling M, Berntsson SG, Alafuzoff I, Lätt J, Larsson EM (2016) Preoperative quantitative MR tractography compared with visual tract evaluation in patients with neuropathologically confirmed gliomas grades II and III: a prospective cohort study. Radiol Res Pract 2016:7671854–7671815. PubMedPubMedCentralGoogle Scholar
  27. 27.
    Zhang H, Wang Y, Lu T, Qiu B, Tang Y, Ou S, Tie X, Sun C, Xu K, Wang Y (2013) Differences between generalized q-sampling imaging and diffusion tensor imaging in the preoperative visualization of the nerve fiber tracts within peritumoral edema in brain. Neurosurgery 73(6):1044–1053; discussion 1053. CrossRefPubMedGoogle Scholar
  28. 28.
    Yeh F-C, Wedeen VJ, Tseng W-YI (2010) Generalized q-sampling imaging. IEEE Trans Med Imaging 29(9):1626–1635. CrossRefPubMedGoogle Scholar
  29. 29.
    Yeh F-C, Verstynen TD, Wang Y, Fernández-Miranda JC, Tseng WYI (2013) Deterministic diffusion fiber tracking improved by quantitative anisotropy. PLoS One 8(11):e80713. CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Abhinav K, Pathak S, Richardson RM, Engh J, Gardner P, Yeh FC, Friedlander RM, Fernandez-Miranda JC (2014) Application of high-definition fiber tractography in the management of supratentorial cavernous malformations: a combined qualitative and quantitative approach. Neurosurgery 74(6):668–680; discussion 680-681. CrossRefPubMedGoogle Scholar
  31. 31.
    Fernandes-Cabral DT, Zenonos GA, Hamilton RL, Panesar SS, Fernandez-Miranda JC (2016) High-definition fiber tractography in the evaluation and surgical planning of Lhermitte-Duclos disease: a case report. World Neurosurg 92:587.e9–587.e13. CrossRefGoogle Scholar
  32. 32.
    Provenzale JM, Mc Graw P, Mhatre P et al (2004) Peritumoral brain regions in gliomas and meningiomas: investigation with isotropic diffusion-weighted MR imaging and diffusion-tensor MR imaging. Radiology 232(2):451–460. CrossRefPubMedGoogle Scholar
  33. 33.
    Stadlbauer A, Nimsky C, Buslei R et al (2007) Diffusion tensor imaging and optimized fiber tracking in glioma patients: histopathologic evaluation of tumor-invaded white matter structures. NeuroImage 34(3):949–956. CrossRefPubMedGoogle Scholar
  34. 34.
    Wei CW, Guo G, Mikulis DJ (2007) Tumor effects on cerebral white matter as characterized by diffusion tensor tractography. Can J Neurol Sci 34:62–68CrossRefPubMedGoogle Scholar
  35. 35.
    Abhinav K, Yeh F-C, Mansouri A, Zadeh G, Fernandez-Miranda JC (2015) High-definition fiber tractography for the evaluation of perilesional white matter tracts in high-grade glioma surgery. Neuro-Oncol 17:1199–1209. PubMedPubMedCentralGoogle Scholar
  36. 36.
    Faust K, Vajkoczy P (2015) Distinct displacements of the optic radiation based on tumor location revealed using preoperative diffusion tensor imaging. J Neurosurg 124(5):1343–1352. CrossRefPubMedGoogle Scholar
  37. 37.
    Akai H, Mori H, Aoki S et al (2005) Diffusion tensor tractography of gliomatosis cerebri: fiber tracking through the tumor. J Comput Assist Tomogr 29(1):127–129. CrossRefPubMedGoogle Scholar
  38. 38.
    Castellano A, Bello L, Michelozzi C et al (2012) Role of diffusion tensor magnetic resonance tractography in predicting the extent of resection in glioma surgery. Neuro-Oncologia 14(2):192–202. CrossRefGoogle Scholar
  39. 39.
    Bello L, Gambini A, Castellano A et al (2008) Motor and language DTI fiber tracking combined with intraoperative subcortical mapping for surgical removal of gliomas. NeuroImage 39(1):369–382. CrossRefPubMedGoogle Scholar
  40. 40.
    Mandonnet E, Capelle L, Duffau H (2006) Extension of paralimbic low grade gliomas: toward an anatomical classification based on white matter invasion patterns. J Neuro-Oncol 78(2):179–185. CrossRefGoogle Scholar
  41. 41.
    Swanson KR, Alvord EC, Murray JD (2000) A quantitative model for differential motility of gliomas in grey and white matter. Cell Prolif 33(5):317–329. CrossRefPubMedGoogle Scholar
  42. 42.
    Lu S, Ahn D, Johnson G, Cha S (2003) Peritumoral diffusion tensor imaging of high-grade gliomas and metastatic brain tumors. AJNR Am J Neuroradiol 24(5):937–941PubMedGoogle Scholar
  43. 43.
    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(6):1258–1271PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Pinar Celtikci
    • 1
  • David T. Fernandes-Cabral
    • 1
  • Fang-Cheng Yeh
    • 1
  • Sandip S. Panesar
    • 1
  • Juan C. Fernandez-Miranda
    • 1
    Email author
  1. 1.Department of Neurological SurgeryUniversity of Pittsburgh Medical CenterPittsburghUSA

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