Skip to main content

Advertisement

SpringerLink
Log in

BOLD fMRI and DTI fiber tracking for preoperative mapping of eloquent cerebral regions in brain tumor patients: impact on surgical approach and outcome

  • Original Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Purpose

Task-based BOLD fMRI and DTI-fiber tracking have become part of the routine presurgical work-up of brain tumor patients in many institutions. However, their potential impact on both surgical treatment and neurologic outcome remains unclear, in despite of the high costs and complex implementation.

Methods

We retrospectively investigated whether performing fMRI and DTI-ft preoperatively substantially impacted surgical planning and patient outcome in a series of brain tumor patients. We assessed (i) the quality of fMRI and DTI-ft results, by using a scale of 0–2 (0 = failed mapping; 1 = intermediate confidence; 2 = good confidence), (ii) whether functional planning substantially contributed to defining the surgical strategy to be undertaken (i.e., no surgery, biopsy, or resection, with or without ESM), the surgical entry point and extent of resection, and (iii) the incidence of neurological deficits post-operatively.

Results

Twenty-seven patients constituted the study population. The mean confidence rating was 1.9/2 for fMRI localization of the eloquent cortex and lateralization of the language function and 1.7/2 for DTI-ft results. Treatment strategy was altered in 33% (9/27) of cases. Surgical entry point was modified in 8% (2/25) of cases. The extent of resection was modified in 40% (10/25). One patient (1/25, 4%) developed one new functional deficit post-operatively.

Conclusion

Functional MR mapping — which must not be considered an alternative to ESM — has a critical role preoperatively, potentially modifying treatment strategy or increasing the neurosurgeons’ confidence in the surgical approach hypothesized based on conventional imaging.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Gil Robles S, Duffau H (2010) Surgical management of World Health Organization Grade II gliomas in eloquent areas: the necessity of preserving a margin around functional structures. Neurosurg Focus 28:E8

    PubMed  Google Scholar 

  2. Duffau H (2013) Brain mapping in tumors: intraoperative or extra-operative? Epilepsia 54(Suppl 9):79–83

    PubMed  Google Scholar 

  3. Duffau H (2012) The challenge to remove diffuse low-grade gliomas while preserving brain functions. Acta Neurochir 154(4):569–574

    PubMed  Google Scholar 

  4. Duffau H, Denvil D, Capelle L (2002) Long term reshaping of language, sensory, and motor maps after glioma resection: a new parameter to integrate in the surgical strategy. J Neurol Neurosurg Psychiatry 72:511–516

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Duffau H, Capelle L, Denvil D, Sichez n, Gatignol P, Lopes M, Mitchell M-C, Sichez J-P, Van Effenterre R, (2003) Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation. J Neurol Neurosurg Psychiatry 74:901–907

    CAS  PubMed  PubMed Central  Google Scholar 

  6. De Witt Hamer PC, Gil Robles S, Zwinderman A, Duffau H, Berger MS (2012) Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J Clin Oncol 30:2559–2565

    PubMed  Google Scholar 

  7. Al R, Brunner P, Schalk G (2018) Electrical stimulation mapping of the brain: basic principles and emerging alternatives. J Clin Neurophysiol 35(2):86–97

    Google Scholar 

  8. Nossek E, Matot I, Shahar T, Barzilai O, Rapoport Y, Gonen T, Sela G, Grossman R, Korn A, Hayat D, Ram Z (2013) Intraoperative seizures during awake craniotomy: incidence and consequences: analysis of 477 patients. Neurosurgery 73:135–140

    PubMed  Google Scholar 

  9. Ogawa S, Lee TM, Kay AR, Tank DW (1990) Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA 87(24):9868–9872

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Huettel SA, Song AW, McCarthy G (2014). Functional magnetic resonance imaging Sinauer, Massachusetts USA

  11. FitzGerald DB, Cosgrove GR, Ronner S, Jiang H, Buchbinder BR, Belliveau JW, Rosen BR, Benson RR (1997) Location of language in the cortex: a comparison between functional MR imaging and electrocortical stimulation. AJNR Am J Neuroradiol 18(8):1529–1539

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Bizzi A, Blasi V, Falini A, Ferroli P, Cadioli M, Danesi U, Aquino D, Marras C, Caldiroli D (2008) Broggi G (2008) Presurgical functional MR imaging of language and motor functions: validation with intraoperative electrocortical mapping. Radiology 248:579–589

    PubMed  Google Scholar 

  13. Tieleman A, Deblaere K, Van Roost D, Van Damne O, Achten E (2009) Preoperative fMRI in tumour surgery. Eur Radiol 19:2523–2534

    PubMed  Google Scholar 

  14. Smits M. Functional magnetic resonance imaging (fMRI) in brain tumor patients. Eur Assoc NeuroOncol Mag 2:123–128

  15. Basser PJ, Pierpaoli C (1998) A simplified method to measure the diffusion tensor from seven MR images. Magn Reson Med 39(6):928–934

    CAS  PubMed  Google Scholar 

  16. 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 USA 96(18):10422–10427

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Mori S, Barker PB (1999) Diffusion in magnetic resonance imaging: its principle and applications. Anat Rec 257(3):102–109

    CAS  PubMed  Google Scholar 

  18. Poupon C, Clark CA, Frouin V, Régis J, Bloch I, Le Bihan D, Mangin J (2000) Regularization of diffusion-based direction maps for the tracking of brain white matter fascicles. Neuroimage 12(2):184–195

    CAS  PubMed  Google Scholar 

  19. Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using DT-MRI data. Magn Reson Med 44(4):625–632

    CAS  PubMed  Google Scholar 

  20. Lee CC, Ward HA, Sharbrough FW, Meyer FB, Marsh WR, Raffel C, So EL, Cascino GD, Shin C, Xu Y, Riederer SJ, Jack CR Jr (1999) Assessment of functional MR imaging in neurosurgical planning. AJNR Am J Neuroradiol 20(8):1511–1519

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Rutten GM, Ramsey NF, van Rijen PC, Noordmans HJ, van Veelen CW (2002) Development of a functional magnetic resonance imaging protocol for intraoperative localization of critical temporoparietal language areas. Ann Neurol 51:350–360

    CAS  PubMed  Google Scholar 

  22. Wilkinson ID, Romanowski CA, Jellinek DA, Morris J, Griffiths PD (2003) Motor functional MRI for pre-operative and intraoperative neurosurgical neurosurgical guidance. Br J Radiol 76(902):98–103

    CAS  PubMed  Google Scholar 

  23. Petrella JR, Shah LM, Harris KM, Friedman AH, George TM, Sampson JH, Pekala JS, Voyvodic JT (2006) Preoperative functional MR imaging localization of language and motor areas: effect on therapeutic decision making in patients with potentially resectable brain tumors. Radiology 240:793–802

    PubMed  Google Scholar 

  24. Tieleman A, Deblaere K, Van Roost D, Van Damme O, Achten E (2009) Preoperative fMRI in tumour surgery. Eur Radiol 19(10):2523–2534

    PubMed  Google Scholar 

  25. Morrison MA, Chruchill NW, Cusimano MD, Schweizer TA, Das S (2016) Graham SJ (2016) Reliability of task-based fMRI fro preoperative planning: a test-retest study in brain tumor patients and healthy controls. PlosOne 11(2):e0149547

    Google Scholar 

  26. Stopa BM, Senders JT, Broekman MLD, Vangel M, Golby AJ (2020) Preoperative functional MRI use in neurooncology patients: a clinician survey. Neurosurg Focus 48(2):E11

    PubMed  PubMed Central  Google Scholar 

  27. Mendez Orellana C, Visch-Brink E, Vernooij M, Kalloe S, Satoer D, Vincent A, van der Lugt A, Smits M (2015) Crossed cerebrocerebellar language lateralization: an additional diagnostic feature for assessing atypical language representation in presurgical functional MR imaging. AJNR Am J Neuroradiol 36(3):518–524

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Carrillo JA, Lai A, Nghiemphu PL, Kim HJ, Phillips HS, Kharbanda S, Moftakhar P, Lalaezari S, Yong W, Ellingson BM, Cloughesy TF, Pope WB (2012) Relationship between tumor enhancement, edema, IDH1 mutational status, MGMT promoter methylation, and survival in glioblastoma. AJNR Am J Neuroradiol 33(7):1349–1355

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Osborn A (2018) Osborn’s Brain Elsevier, Philadelphia

  30. Zabramski JM, Wascher TM, Spetzler RF, Johnson B, Golfinos J, Drayer BP, Brown B, Rigamonti D, Brown G (1994) The natural history of familial cavernous malformations: results of an ongoing study. J Neurosurg 80(3):422–432

    CAS  PubMed  Google Scholar 

  31. Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW (2016) The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathol 131(6):803–820

    PubMed  Google Scholar 

  32. Ellingson BM, Bendszus M, Boxerman J, Barboriak D, Erickson BJ, Smits M, Nelson SJ, Gerstner E, Alexander B, Goldmacher G, Wick W, Vogelbaum M, Weller M, Galanis E, Kalpathy-Cramer J, Shankar L, Jacobs P, Pope WB, Yang D, Chung C, Knopp MV, Cha S, van den Bent MJ, Chang S, Yung WK, Cloughesy TF, Wen PY, Gilbert MR; Jumpstarting Brain Tumor Drug Development Coalition Imaging Standardization Steering Committee (2015) Consensus recommendations for a standardized Brain Tumor Imaging Protocol in clinical trials Neuro Oncol 17(9):1188–1198

  33. Friston KJ, Frith C, Frackowiak RS et al (1995) Characterizing dynamic brain responses with fMRI: a multivariate approach. Neuroimage 2:166–172

    CAS  PubMed  Google Scholar 

  34. Penfield W, Boldrey E (1937) Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60(4):389–443

    Google Scholar 

  35. Wernicke C. Der aphasische Symptomenkomplex. Breslau: Cohn, Weigert,1974

  36. Geschwind N (1971) Aphasia. N Engl J Med 284:654–656

    CAS  PubMed  Google Scholar 

  37. Benson DF, Geschwind N (1985) Aphasia and related disorders: a clinical approach. In: Mesulam MM (ed), Principles of behavioral and cognitive neurology, EA Davis Philadelphia, pp 193–238

  38. Mayeux R, Kandel R (1985) Natural language, disorders of language, and other localizable disorders of cognitive function. In: Kandel ER, Schwartz J (eds) Principles of neural science. Elsevier New York, pp 688–703

  39. Basser PJ, Mattiello J, LeBihan D (1994) MR diffusion tensor spectroscopy and imaging. Biophys J 66(1):259–267

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 6(6):893–906

    Google Scholar 

  41. Jones DK, Horsfield MA, Simmons A (1999) Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magn Reson Med 42(3):515–525

    CAS  PubMed  Google Scholar 

  42. Warrington S, Bryant KL, Khrapitchev AA, Sallet J, Charquero-Ballester M, Jbabdi S, Mars RB, Sotiropoulos SN (2020) XTRACT - standardised protocols for automated tractography in the human and macaque brain. Neuroimage 217:116923

    PubMed  Google Scholar 

  43. Krings T, Reinges MH, Erberich S, Kemeny S, Rohde V, Spetzger U, Korinth M, Willmes K, Gilsbach JM, Thron A (2001) Functional MRI for presurgical planning: problems, artefacts, and solution strategies. J Neurorol Neurosurg Psychiatry 70:749–760

    CAS  Google Scholar 

  44. Lolli V, Rovai A, Trotta N, Goldman S, Sadeghi N, Lefranc F, Jousmäki V, De Tiège X (2021) Pneumatic artificial muscle-based stimulator for passive functional magnetic resonance imaging sensorimotor mapping in patients with brain tumours. J Neurosci Methods 359:109227

    PubMed  Google Scholar 

  45. Guzzetta A, Staudt M, Petacchi E, Ehlers J, Erb M, Wilke M, Krägeloh-Mann I, Cioni G (2007) Brain representation of active and passive hand movements in children. Pediatr Res 61:485–490

    PubMed  Google Scholar 

  46. Kocak M, Ulmer JL, Sahin Ugurel M, Gaggl V, Prost RW (2009) Motor homunculus: passive mapping in healthy volunteers by using functional MR imaging – initial results. Radiology 251:485–492

    PubMed  Google Scholar 

  47. Boscolo Galazzo I, Storti SF, Formaggio E, Pizzini FB, Fiaschi A, Beltramello A, Bertoldo A, Manganotti P (2014) Investigation of brain hemodynamic changes induced by active and passive movements: a combined arterial spin labeling–BOLD fMRI study. J Magn Reson Imaging 40:937–948

    PubMed  Google Scholar 

  48. Choudhri AF, Patel RM, Siddiqui A, Whitehead MT, Wheless JW (2015) Cortical activation through passive-motion functional MRI. AJNR Am J Neuroradiol 36:1675–1681

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Hajnal J, Myers R, Oatridge A, Schwieso JE, Young IR, Bydder GM (1994) Artefacts due to stimulus correlated motion in functional imaging of the brain. Magn Res Med 31:283–291

    CAS  Google Scholar 

  50. Friston KJ, Williams S, Howard R, Frackowiak RS, Turner R (1996) Movement-related effects in fMRI time-series. Magn Reson Med 35:346–355

    CAS  PubMed  Google Scholar 

  51. Bullmore ET, Brammer MJ, Rabe-Hesketh S, Curtis VA, Morris RG, Williams SC, Sharma T, McGuire PK (1999) Methods for diagnosis and treatment of stimulus-correlated motion in generic brain activation studies using fMRI. Hum Brain Map 7:38–48

    CAS  Google Scholar 

  52. Seto E, Sela G, McIlroy W, Black SE, Staines WR, Bronskill MJ, McIntosh AR, Graham SJ (2001) Quantifying head motion associated with motor tasks used in fMRI. Neuroimage 14:284–297

    CAS  PubMed  Google Scholar 

  53. Tie Y, Rigolo L, Norton IH, Huang RY, Wu W, Orringer D, Mukundan S Jr, Golby AJ (2014) Defining language networks from resting-state fMRI for surgical planning - a feasibility study. Hum Brain Mapp 35(3):1018–1030

    PubMed  Google Scholar 

  54. Branco P, Seixas D, Deprez S, Kovacs S, Peeters R, Castro SL, Sunaert S (2016) Resting-state functional magnetic resonance imaging for language preoperative planning. Front Hum Neurosci 10:1–14

    Google Scholar 

  55. Sair HI, Yahyavi-Firouz-Abadi N, Calhoun VD, Airan RD, Agarwal S, Intrapiromkul J, Choe AS, Gujar SK, Caffo B, Lindquist MA, Pillai JJ (2016) Presurgical brain mapping of the language network in patients with brain tumors using resting-state fMRI: comparison with task fMRI. Hum Brain Mapp 37(3):913–923

  56. McRobbie D, Semple S. Quality control and artefacts in magnetic resonance imaging (2017), IPEM

  57. Pomper MG, Port JD (2000) New techniques in MR imaging of brain tumors. Magn Reson Imaging Clin N Am 8(4):691–713

    CAS  PubMed  Google Scholar 

  58. Sunaert S (2006) Presurgical planning for tumor resectioning. J Magn Reson Imaging 223:887–905

    Google Scholar 

  59. Jones DK, Pierpaoli C (2005) Confidence mapping in diffusion tensor magnetic resonance imaging tractography using a bootstrap approach. Magn Reson Med 53(5)_1143–1149

  60. Roux FE, Boulanouar K, Lotterie JA, Mejdoubi M, LeSage JP, Berry I (2003) Language functional magnetic resonance imaging in preoperative assessment of language areas: correlation with direct cortical stimulation. Neurosurgery 52:1335–1345

    PubMed  Google Scholar 

  61. Luna LP, Sherbaf FG, Sair HI, Mukkerjee D, Oliveira IB, Köhler CA (2021) Can preoperative mapping with functional MRI reduce morbidity in brain tumor resection? A systematic review and meta-analysis of 68 observational studies. Radiology 300:338–349

    PubMed  Google Scholar 

Download references

Acknowledgements

The authors wish to express their heartfelt gratitude to the MRI physicists Professor Thierry Metens and Dr. Julie Absil and to the MR technologists of the Radiology Department without whom this work would not have been possible.

Funding

Valentina Lolli was supported by the Fonds Erasme pour la Recherche Médicale (Brussels, Belgium). Tim Coolen was supported by the Fonds de Recherche Scientifique (FNRS, Fédération Wallonie Bruxelles de Belgique) and by the Fonds Erasme pour la Recherche Médicale (Brussels, Belgium).

Author information

Author notes

  1. Valentina Lolli and Tim Coolen contributed equally to this work.

Authors and Affiliations

  1. Department of Radiology, CUB - Hôpital Erasme, Brussels, Belgium

    Valentina Elisabetta Lolli, Tim Coolen & Niloufar Sadeghi

  2. Department of Neurology, CUB - Hôpital Erasme, Brussels, Belgium

    Philippe Voordecker

  3. Department of Neurosurgery, CUB - Hôpital Erasme, Brussels, Belgium

    Florence Lefranc

Authors
  1. Valentina Elisabetta Lolli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tim Coolen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Niloufar Sadeghi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Philippe Voordecker
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Florence Lefranc
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Valentina Lolli: conceptualization, investigation, methodology, writing — original draft, writing — review and editing, visualization.

Tim Coolen: conceptualization, investigation, methodology, writing — original draft, writing — review and editing, visualization

Niloufar Sadeghi: writing — review and editing, supervision

Philippe Voordecker: investigation, writing — review and editing

Florence Lefranc: conceptualization, investigation, writing — review and editing, validation, supervision

Corresponding author

Correspondence to Valentina Elisabetta Lolli.

Ethics declarations

Ethical approval

The study was approved by the CUB-Hôpital Erasme Ethics Committee (P2021/372) and was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. Written consent for publication was obtained in 17/27 patients who had been priorly enrolled in two different research projects (Ref: CUB-Hôpital Erasme Ethics Committee P2016/515 and P2017/272) which allowed use of anonymized data for ulterior publications. Patient consent waiver was granted by the CUB-Hôpital Erasme Ethics Committee (P2021/372) for the remaining 10/27 patients.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lolli, V.E., Coolen, T., Sadeghi, N. et al. BOLD fMRI and DTI fiber tracking for preoperative mapping of eloquent cerebral regions in brain tumor patients: impact on surgical approach and outcome. Neurol Sci 44, 2903–2914 (2023). https://doi.org/10.1007/s10072-023-06667-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-023-06667-2

Keywords

Search

Navigation