Functional DTI tractography in brainstem cavernoma surgery

View More View Less
  • 1 Department of Neurosurgery, Charité–Universitätsmedizin Berlin, Germany
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00
Print or Print + Online

OBJECTIVE

Surgical resection of brainstem cavernomas is associated with high postoperative morbidity due to the density of local vulnerable structures. Classical mapping of pathways by diffusion tensor imaging (DTI) has proven to be unspecific and confusing in many cases. In the current study, the authors aimed to establish a more reliable, specific, and objective method for somatotopic visualization of the descending motor pathways with navigated transcranial magnetic stimulation (nTMS)–based DTI fiber tracking.

METHODS

Twenty-one patients with brainstem cavernomas were examined with nTMS prior to surgery. The resting motor threshold (RMT) and cortical representation areas of hand, leg, and facial function were determined on both hemispheres. Motor evoked potential (MEP)–positive stimulation spots were then set as seed points for tractography. Somatotopic fiber tracking was performed at a fractional anisotropy (FA) value of 75% of the individual FA threshold.

RESULTS

Mapping of the motor cortex and tract reconstruction for hand, leg, and facial function was successful in all patients. The somatotopy of corticospinal and corticonuclear tracts was also clearly depicted on the brainstem level. Higher preoperative RMT values were associated with a postoperative motor deficit (p < 0.05) and correlated with a lower FA threshold (p < 0.05), revealing structural impairment of the corticospinal tract (CST) prior to surgery. In patients with a new deficit, the distance between the lesion and CST was below 1 mm.

CONCLUSIONS

nTMS-based fiber tracking enables objective somatotopic tract visualization on the brainstem level and provides a valuable instrument for preoperative planning, intraoperative orientation, and individual risk stratification. nTMS may thus increase the safety of surgical resection of brainstem cavernomas.

ABBREVIATIONS

BSCM = brainstem cavernous malformation; CBT = corticobulbar tract; CST = corticospinal tract; DTI = diffusion tensor imaging; DTT = diffusion tensor tractography; FA = fractional anisotropy; FAT = FA threshold; FDI = first digital interosseus muscle; MEP = motor evoked potential; MRC = Medical Research Council; mRS = modified Rankin Scale; nTMS = navigated transcranial magnetic stimulation; RMT = resting motor threshold; ROI = region of interest.

Artist’s illustration of the classic mulberry appearance of a cavernoma. This illustration represents the Seven Cavernomas series by Dr. Michael Lawton, a collection of articles defining the tenets and techniques for the treatment of cavernous malformations, a taxonomy for classifying these lesions, and the nuances of their surgical approaches. Artist: Peter M. Lawrence. Used with permission from Barrow Neurological Institute, Phoenix, Arizona. See the article by Garcia et al. (pp 671–682).

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00

Contributor Notes

Correspondence Peter Vajkoczy: Charité–Universitätsmedizin Berlin, Germany. peter.vajkoczy@charite.de.

INCLUDE WHEN CITING Published online December 25, 2020; DOI: 10.3171/2020.7.JNS20403.

Disclosures T. Picht has served as a speaker for Nexstim Oy but is not a contracted consultant.

  • 1

    Gross BA , Lin N , Du R , Day AL . The natural history of intracranial cavernous malformations . Neurosurg Focus . 2011 ;30 (6 ):E24 .

    • Search Google Scholar
    • Export Citation
  • 2

    Kim PY , Park YG , Choi JU , et al. An analysis of the natural history of cavernous malformations . Surg Neurol . 1997 ;48 (1 ):9 18 .

    • Search Google Scholar
    • Export Citation
  • 3

    Robinson JR Jr , Awad IA , Little JR . Natural history of the cavernous angioma . J Neurosurg . 1991 ;75 (5 ):709 714 .

  • 4

    Dukatz T , Sarnthein J , Sitter H , et al. Quality of life after brainstem cavernoma surgery in 71 patients . Neurosurgery . 2011 ;69 (3 ):689 695 .

    • Search Google Scholar
    • Export Citation
  • 5

    Hauck EF , Barnett SL , White JA , Samson D . Symptomatic brainstem cavernomas . Neurosurgery . 2009 ;64 (1 ):61 71 .

  • 6

    Gross BABH , Batjer HH , Awad IA , Bendok BR . Brainstem cavernous malformations . Neurosurgery . 2009 ;64 (5 ):E805 E818 .

  • 7

    Gross BA , Batjer HH , Awad IA , et al. Brainstem cavernous malformations: 1390 surgical cases from the literature . World Neurosurg . 2013 ;80 (1-2 ):89 93 .

    • Search Google Scholar
    • Export Citation
  • 8

    Cao Z , Lv J , Wei X , Quan W . Appliance of preoperative diffusion tensor imaging and fiber tractography in patients with brainstem lesions . Neurol India . 2010 ;58 (6 ):886 890 .

    • Search Google Scholar
    • Export Citation
  • 9

    Berman J. Diffusion MR tractography as a tool for surgical planning . Magn Reson Imaging Clin N Am . 2009 ;17 (2 ):205 214 .

  • 10

    Sarubbo S , De Benedictis A , Merler S , et al. Towards a functional atlas of human white matter . Hum Brain Mapp . 2015 ;36 (8 ):3117 3136 .

    • Search Google Scholar
    • Export Citation
  • 11

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

  • 12

    Sundgren PC , Dong Q , Gómez-Hassan D , et al. Diffusion tensor imaging of the brain: review of clinical applications . Neuroradiology . 2004 ;46 (5 ):339 350 .

    • Search Google Scholar
    • Export Citation
  • 13

    Basser PJ , Pajevic S , Pierpaoli C , et al. In vivo fiber tractography using DT-MRI data . Magn Reson Med . 2000 ;44 (4 ):625 632 .

  • 14

    Chen X , Weigel D , Ganslandt O , et al. Diffusion tensor-based fiber tracking and intraoperative neuronavigation for the resection of a brainstem cavernous angioma . Surg Neurol . 2007 ;68 (3 ):285 291 .

    • Search Google Scholar
    • Export Citation
  • 15

    Faraji AH , Abhinav K , Jarbo K , et al. Longitudinal evaluation of corticospinal tract in patients with resected brainstem cavernous malformations using high-definition fiber tractography and diffusion connectometry analysis: preliminary experience . J Neurosurg . 2015 ;123 (5 ):1133 1144 .

    • Search Google Scholar
    • Export Citation
  • 16

    Flores BC , Whittemore AR , Samson DS , Barnett SL . The utility of preoperative diffusion tensor imaging in the surgical management of brainstem cavernous malformations . J Neurosurg . 2015 ;122 (3 ):653 662 .

    • Search Google Scholar
    • Export Citation
  • 17

    Li D , Jiao YM , Wang L , et al. Surgical outcome of motor deficits and neurological status in brainstem cavernous malformations based on preoperative diffusion tensor imaging: a prospective randomized clinical trial . J Neurosurg . 2018 ;130 (1 ):286 301 .

    • Search Google Scholar
    • Export Citation
  • 18

    Ulrich NH , Kockro RA , Bellut D , et al. Brainstem cavernoma surgery with the support of pre- and postoperative diffusion tensor imaging: initial experiences and clinical course of 23 patients . Neurosurg Rev . 2014 ;37 (3 ):481 492 .

    • Search Google Scholar
    • Export Citation
  • 19

    Januszewski J , Albert L , Black K , Dehdashti AR . The usefulness of diffusion tensor imaging and tractography in surgery of brainstem cavernous malformations . World Neurosurg . 2016 ;93 :377 388 .

    • Search Google Scholar
    • Export Citation
  • 20

    Ruohonen J , Karhu J . Navigated transcranial magnetic stimulation . Neurophysiol Clin . 2010 ;40 (1 ):7 17 .

  • 21

    Picht T , Mularski S , Kuehn B , et al. Navigated transcranial magnetic stimulation for preoperative functional diagnostics in brain tumor surgery . Neurosurgery . 2009 ;65 (6 )(suppl):93 99 .

    • Search Google Scholar
    • Export Citation
  • 22

    Lefaucheur JP , Picht T . The value of preoperative functional cortical mapping using navigated TMS . Neurophysiol Clin . 2016 ;46 (2 ):125 133 .

    • Search Google Scholar
    • Export Citation
  • 23

    Picht T , Schmidt S , Brandt S , et al. Preoperative functional mapping for rolandic brain tumor surgery: comparison of navigated transcranial magnetic stimulation to direct cortical stimulation . Neurosurgery . 2011 ;69 (3 ):581 588 .

    • Search Google Scholar
    • Export Citation
  • 24

    Picht T . Current and potential utility of transcranial magnetic stimulation in the diagnostics before brain tumor surgery . CNS Oncol . 2014 ;3 (4 ):299 310 .

    • Search Google Scholar
    • Export Citation
  • 25

    Krieg SM , Shiban E , Buchmann N , et al. Utility of presurgical navigated transcranial magnetic brain stimulation for the resection of tumors in eloquent motor areas . J Neurosurg . 2012 ;116 (5 ):994 1001 .

    • Search Google Scholar
    • Export Citation
  • 26

    Frey D , Strack V , Wiener E , et al. A new approach for corticospinal tract reconstruction based on navigated transcranial stimulation and standardized fractional anisotropy values . Neuroimage . 2012 ;62 (3 ):1600 1609 .

    • Search Google Scholar
    • Export Citation
  • 27

    Jussen D , Zdunczyk A , Schmidt S , et al. Motor plasticity after extra-intracranial bypass surgery in occlusive cerebrovascular disease . Neurology . 2016 ;87 (1 ):27 35 .

    • Search Google Scholar
    • Export Citation
  • 28

    Awiszus F , Feistner H , Urbach D , Bostock H . Characterisation of paired-pulse transcranial magnetic stimulation conditions yielding intracortical inhibition or I-wave facilitation using a threshold-hunting paradigm . Exp Brain Res . 1999 ;129 (2 ):317 324 .

    • Search Google Scholar
    • Export Citation
  • 29

    Nimsky C , Ganslandt O , Merhof D , et al. Intraoperative visualization of the pyramidal tract by diffusion-tensor-imaging-based fiber tracking . Neuroimage . 2006 ;30 (4 ):1219 1229 .

    • Search Google Scholar
    • Export Citation
  • 30

    Rosenstock T , Giampiccolo D , Schneider H , et al. Specific DTI seeding and diffusivity-analysis improve the quality and prognostic value of TMS-based deterministic DTI of the pyramidal tract . Neuroimage Clin . 2017 ;16 :276 285 .

    • Search Google Scholar
    • Export Citation
  • 31

    Kovanlikaya I , Firat Z , Kovanlikaya A , et al. Assessment of the corticospinal tract alterations before and after resection of brainstem lesions using diffusion tensor imaging (DTI) and tractography at 3T . Eur J Radiol . 2011 ;77 (3 ):383 391 .

    • Search Google Scholar
    • Export Citation
  • 32

    Rosenstock T , Grittner U , Acker G , et al. Risk stratification in motor area-related glioma surgery based on navigated transcranial magnetic stimulation data . J Neurosurg . 2017 ;126 (4 ):1227 1237 .

    • Search Google Scholar
    • Export Citation
  • 33

    Cantu C , Murillo-Bonilla L , Arauz A , et al. Predictive factors for intracerebral hemorrhage in patients with cavernous angiomas . Neurol Res . 2005 ;27 (3 ):314 318 .

    • Search Google Scholar
    • Export Citation
  • 34

    Pandey P , Westbroek EM , Gooderham PA , Steinberg GK . Cavernous malformation of brainstem, thalamus, and basal ganglia: a series of 176 patients . Neurosurgery . 2013 ;72 (4 ):573 589 .

    • Search Google Scholar
    • Export Citation
  • 35

    Garcia RM , Ivan ME , Lawton MT . Brainstem cavernous malformations: surgical results in 104 patients and a proposed grading system to predict neurological outcomes . Neurosurgery . 2015 ;76 (3 ):265 278 .

    • Search Google Scholar
    • Export Citation
  • 36

    Walcott BP , Choudhri O , Lawton MT . Brainstem cavernous malformations: Natural history versus surgical management . J Clin Neurosci . 2016 ;32 :164 165 .

    • Search Google Scholar
    • Export Citation
  • 37

    Mori S , van Zijl PC . Fiber tracking: principles and strategies—a technical review . NMR Biomed . 2002 ;15 (7-8 ):468 480 .

  • 38

    Leclercq D , Delmaire C , de Champfleur NM , et al. Diffusion tractography: methods, validation and applications in patients with neurosurgical lesions . Neurosurg Clin N Am . 2011 ;22 (2 ):253 268 , ix .

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 298 298 298
Full Text Views 88 88 88
PDF Downloads 130 130 130
EPUB Downloads 0 0 0