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Anatomo-radiological correlation between diffusion tensor imaging and histologic analyses of glial tumors: a preliminary study

  • Original Article - Brain Tumors
  • Published:
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Abstract

Background and purpose

The challenge of the neurosurgical management of gliomas lies in achieving a maximal resection without persistent functional deficit. Diffusion tensor imaging (DTI) allows non-invasive identification of white matter tracts and their interactions with the tumor. Previous DTI validation studies were compared with intraoperative cortical stimulation, but none was performed based on the tumor anatomopathological analysis. This preliminary study evaluates the correlation between the preoperative subcortical DTI tractography and histology in terms of fiber direction as well as potential tumor-related fiber disruption.

Methods

Eleven patients harboring glial tumors underwent preoperative DTI images. Correlations were performed between the visual color-coded anisotropy (FA) map analysis and the tumor histology after “en bloc” resection. Thirty-one tumor areas were classified according to the degree of tumor infiltration, the destruction of myelin fibers and neurofilaments, the presence of organized white matter fibers, and their orientation in space.

Results

After histologic comparison, the DTI sensitivity and specificity to predict disrupted fiber tracts were respectively of 89% and 90%. The positive and negative predicted values of DTI were 80% and 95%. The DTI data were in line with the histologic myelin fiber orientation in 90% of patients. In our series, the prevalence of destructed fiber was 31%. Glioblastoma WHO grade IV harbored a higher proportion of destructed white matter tracts. Lower WHO grades were associated with higher preservation of subcortical fiber tracts.

Conclusion

This DTI/histology study of “en bloc”–resected gliomas reported a high and reproducible concordance of the visual color-coded FA map with the histologic examination to predict subcortical fiber tract disruption. Our series brought consistency to the DTI data that could be performed routinely for glioma surgery to predict the tumor grade and the postoperative clinical outcomes.

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Abbreviations

DTI:

Diffusion tensor imaging

MBP:

Myelin basic protein

ROI:

Region of interest

FA map:

Fractional anisotropy map

References

  1. Atlas SW, Grossman RI, Hackney DB, Gomori JM, Campagna N, Goldberg HI, Bilaniuk LT, Zimmerman RA (1988) Calcified intracranial lesions: detection with gradient-echo-acquisition rapid MR imaging. AJR Am J Roentgenol 150(6):1383–1389

    Article  CAS  PubMed  Google Scholar 

  2. Baheza RA, Welch EB, Gochberg DF, Sanders M, Harvey S, Gore JC, Yankeelov TE (2015) Detection of microcalcifications by characteristic magnetic susceptibility effects using MR phase image cross-correlation analysis. Med Phys 42(3):1436–1452

    Article  PubMed  PubMed Central  Google Scholar 

  3. 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

    Article  PubMed  Google Scholar 

  4. Bucci M, Mandelli ML, Berman JI, Amirbekian B, Nguyen C, Berger MS, Henry RG (2013) Quantifying diffusion MRI tractography of the corticospinal tract in brain tumors with deterministic and probabilistic methods. Neuroimage Clin 3:361–368

    Article  PubMed  PubMed Central  Google Scholar 

  5. Budde MD, Annese J (2013) Quantification of anisotropy and fiber orientation in human brain histological sections. Front Integr Neurosci 7:3

    Article  PubMed  PubMed Central  Google Scholar 

  6. Chen W, Zhu W, Kovanlikaya I, Kovanlikaya A, Liu T, Wang S, Salustri C, Wang Y (2014) Intracranial calcifications and hemorrhages: characterization with quantitative susceptibility mapping. Radiology 270(2):496–505

    Article  PubMed  PubMed Central  Google Scholar 

  7. 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(3):1601–1608

    Article  PubMed  Google Scholar 

  8. Conturo TE, Lori NF, Cull TS, Akbudak E, Snyder AZ, Shimony JS, McKinstry RC, Burton H, Raichle ME (1999) Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci U S A 96(18):10422–10427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Duffau H (2005) Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity. Lancet Neurol 4(8):476–486

    Article  PubMed  Google Scholar 

  10. Duffau H (2007) Contribution of cortical and subcortical electrostimulation in brain glioma surgery: methodological and functional considerations. Neurophysiologie Clinique/Clinical Neurophysiology 37(6):373–382

    Article  CAS  PubMed  Google Scholar 

  11. Duffau H (2014) The dangers of magnetic resonance imaging diffusion tensor tractography in brain surgery. World Neurosurg 81(1):56–58

    Article  PubMed  Google Scholar 

  12. Duffau H, Mandonnet E (2013) The “onco-functional balance” in surgery for diffuse low-grade glioma: integrating the extent of resection with quality of life. Acta Neurochir 155(6):951–957

    Article  PubMed  Google Scholar 

  13. 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

    Article  PubMed  Google Scholar 

  14. Gangolli M, Holleran L, Hee Kim J, Stein TD, Alvarez V, McKee AC, Brody DL (2017) Quantitative validation of a nonlinear histology-MRI coregistration method using generalized Q-sampling imaging in complex human cortical white matter. Neuroimage 153:152–167

    Article  PubMed  PubMed Central  Google Scholar 

  15. Henderson F, Abdullah KG, Verma R, Brem S (2020) Tractography and the connectome in neurosurgical treatment of gliomas: the premise, the progress, and the potential. Neurosurg Focus 48(2):E6

    Article  PubMed  Google Scholar 

  16. Kier EL, Staib LH, Davis LM, Bronen RA (2004) MR imaging of the temporal stem: anatomic dissection tractography of the uncinate fasciculus, inferior occipitofrontal fasciculus, and Meyer’s loop of the optic radiation. AJNR Am J Neuroradiol 25(5):677–691

    PubMed  Google Scholar 

  17. Lawes INC, Barrick TR, Murugam V, Spierings N, Evans DR, Song M, Clark CA (2008) Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection. NeuroImage 39(1):62–79

    Article  PubMed  Google Scholar 

  18. Leclercq D, Delmaire C, Menjot de Champfleur N, Chiras J, Lehéricy S (2011) Diffusion tractography: methods, validation and applications in patients with neurosurgical lesions. Neurosurg Clin N Am 22(2):253–268

    Article  PubMed  Google Scholar 

  19. Leclercq D, Duffau H, Delmaire C, Capelle L, Gatignol P, Ducros M, Chiras J, Lehéricy S (2010) Comparison of diffusion tensor imaging tractography of language tracts and intraoperative subcortical stimulations: clinical article. J Neurosurg 112(3):503–511

    Article  PubMed  Google Scholar 

  20. Mandonnet E, Winkler PA, Duffau H (2010) Direct electrical stimulation as an input gate into brain functional networks: principles, advantages and limitations. Acta Neurochir 152(2):185–193

    Article  PubMed  Google Scholar 

  21. Martino J, De Witt Hamer PC, Berger MS, Lawton MT, Arnold CM, de Lucas EM, Duffau H (2013) Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study. Brain Struct Funct 218(1):105–121

    Article  PubMed  Google Scholar 

  22. 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(2):265–269

    Article  CAS  PubMed  Google Scholar 

  23. Mori S, Frederiksen K, van Zijl PCM, Stieltjes B, Kraut MA, Solaiyappan M, Pomper MG (2002) Brain white matter anatomy of tumor patients evaluated with diffusion tensor imaging. Ann Neurol 51(3):377–380

    Article  PubMed  Google Scholar 

  24. Morita N, Wang S, Kadakia P, Chawla S, Poptani H, Melhem ER (2011) Diffusion tensor imaging of the corticospinal tract in patients with brain neoplasms. Magn Reson Med Sci 10(4):239–243

    Article  PubMed  Google Scholar 

  25. Mormina E, Longo M, Arrigo A, Alafaci C, Tomasello F, Calamuneri A, Marino S, Gaeta M, Vinci SL, Granata F (2015) MRI Tractography of corticospinal tract and arcuate fasciculus in high-grade gliomas performed by constrained spherical deconvolution: qualitative and quantitative analysis. AJNR Am J Neuroradiol 36(10):1853–1858

    Article  CAS  PubMed  Google Scholar 

  26. Nimsky C, Ganslandt O, Cerny S, Hastreiter P, Greiner G, Fahlbusch R (2000) Quantification of, visualization of, and compensation for brain shift using intraoperative magnetic resonance imaging. Neurosurgery 47(5):1070–1079 discussion 1079-1080

    Article  CAS  PubMed  Google Scholar 

  27. Ohue S, Kohno S, Inoue A, Yamashita D, Harada H, Kumon Y, Kikuchi K, Miki H, Ohnishi T (2012) Accuracy of diffusion tensor magnetic resonance imaging-based tractography for surgery of gliomas near the pyramidal tract: a significant correlation between subcortical electrical stimulation and postoperative tractography. Neurosurgery 70(2):283–294

    Article  PubMed  Google Scholar 

  28. Pajevic S, Pierpaoli C (1999) Color schemes to represent the orientation of anisotropic tissues from diffusion tensor data: application to white matter fiber tract mapping in the human brain. Magn Reson Med 42(3):526–540

    Article  CAS  PubMed  Google Scholar 

  29. Pallud J, Rigaux-Viode O, Corns R, Muto J, Lopez Lopez C, Mellerio C, Sauvageon X, Dezamis E (2017) Direct electrical bipolar electrostimulation for functional cortical and subcortical cerebral mapping in awake craniotomy. Practical considerations. Neurochirurgie 63(3):164–174

    Article  CAS  PubMed  Google Scholar 

  30. Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G (1996) Diffusion tensor MR imaging of the human brain. Radiology 201(3):637–648

    Article  CAS  PubMed  Google Scholar 

  31. Pujol S, Wells W, Pierpaoli C et al (2015) The DTI challenge: toward standardized evaluation of diffusion tensor imaging tractography for neurosurgery: the DTI challenge on tractography for neurosurgery. J Neuroimaging 25(6):875–882

    Article  PubMed  PubMed Central  Google Scholar 

  32. Reinges MHT, Nguyen H-H, Krings T, Hütter B-O, Rohde V, Gilsbach JM (2004) Course of brain shift during microsurgical resection of supratentorial cerebral lesions: limits of conventional neuronavigation. Acta Neurochir 146(4):369–377 discussion 377

    Article  CAS  PubMed  Google Scholar 

  33. Reyns N, Leroy H-A, Delmaire C, Derre B, Le-Rhun E, Lejeune J-P (2017) Intraoperative MRI for the management of brain lesions adjacent to eloquent areas. Neurochirurgie 63(3):181–188

    Article  CAS  PubMed  Google Scholar 

  34. Spena G, Nava A, Cassini F et al (2010) Preoperative and intraoperative brain mapping for the resection of eloquent-area tumors. A prospective analysis of methodology, correlation, and usefulness based on clinical outcomes. Acta Neurochir 152(11):1835–1846

    Article  PubMed  Google Scholar 

  35. 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(3):803–810

    Article  PubMed  Google Scholar 

  36. 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(3):949–956

    Article  PubMed  Google Scholar 

  37. 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(3):462–469

    PubMed  CAS  Google Scholar 

  38. 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

    Article  PubMed  Google Scholar 

  39. Young RJ, Tan ET, Peck KK et al (2017) Comparison of compressed sensing diffusion spectrum imaging and diffusion tensor imaging in patients with intracranial masses. Magn Reson Imaging 36:24–31

    Article  PubMed  Google Scholar 

  40. Zhang J, van Zijl PCM, Laterra J, Salhotra A, Lal B, Mori S, Zhou J (2007) Unique patterns of diffusion directionality in rat brain tumors revealed by high-resolution diffusion tensor MRI. Magn Reson Med 58(3):454–462

    Article  PubMed  PubMed Central  Google Scholar 

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Author information

Authors and Affiliations

  1. Department of Neurosurgery, CHU Lille, Univ. Lille, F-59000, Lille, France

    Henri-Arthur Leroy, B. Derré, M. Baroncini & N. Reyns

  2. Inserm, CHU Lille, U1189 - ONCO-THAI - Image Assisted Laser Therapy for Oncology, Univ. Lille, F-59000, Lille, France

    Henri-Arthur Leroy & N. Reyns

  3. Department of Neuroradiology, CHU Lille, Univ. Lille, F-59000, Lille, France

    M. Lacoste & C. Delmaire

  4. Department of Anatomopathology, CHU Lille, Univ. Lille, F-59000, Lille, France

    C-A. Maurage

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  1. Henri-Arthur Leroy
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  2. M. Lacoste
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  3. C-A. Maurage
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Correspondence to Henri-Arthur Leroy.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee (name of institute/committee) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Leroy, HA., Lacoste, M., Maurage, CA. et al. Anatomo-radiological correlation between diffusion tensor imaging and histologic analyses of glial tumors: a preliminary study. Acta Neurochir 162, 1663–1672 (2020). https://doi.org/10.1007/s00701-020-04323-8

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  • DOI: https://doi.org/10.1007/s00701-020-04323-8

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