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Quantifying diffusion MRI tractography of the corticospinal tract in brain tumors with deterministic and probabilistic methods.

Bucci M, Mandelli ML, Berman JI, Amirbekian B, Nguyen C, Berger MS, Henry RG - Neuroimage Clin (2013)

Bottom Line: The probabilistic q-ball fiber tractography was significantly better than DTI methods in terms of sensitivity and accuracy of the course through the white matter.The provided data show that probabilistic HARDI tractography is the most objective and reproducible analysis but given the small sample and number of stimulation points a generalization about our results should be given with caution.Indeed our results inform the capabilities of preoperative diffusion fiber tracking and indicate that such data should be used carefully when making pre-surgical and intra-operative management decisions.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, University of California, San Francisco, CA, USA.

ABSTRACT

Introduction: Diffusion MRI tractography has been increasingly used to delineate white matter pathways in vivo for which the leading clinical application is presurgical mapping of eloquent regions. However, there is rare opportunity to quantify the accuracy or sensitivity of these approaches to delineate white matter fiber pathways in vivo due to the lack of a gold standard. Intraoperative electrical stimulation (IES) provides a gold standard for the location and existence of functional motor pathways that can be used to determine the accuracy and sensitivity of fiber tracking algorithms. In this study we used intraoperative stimulation from brain tumor patients as a gold standard to estimate the sensitivity and accuracy of diffusion tensor MRI (DTI) and q-ball models of diffusion with deterministic and probabilistic fiber tracking algorithms for delineation of motor pathways.

Methods: We used preoperative high angular resolution diffusion MRI (HARDI) data (55 directions, b = 2000 s/mm(2)) acquired in a clinically feasible time frame from 12 patients who underwent a craniotomy for resection of a cerebral glioma. The corticospinal fiber tracts were delineated with DTI and q-ball models using deterministic and probabilistic algorithms. We used cortical and white matter IES sites as a gold standard for the presence and location of functional motor pathways. Sensitivity was defined as the true positive rate of delineating fiber pathways based on cortical IES stimulation sites. For accuracy and precision of the course of the fiber tracts, we measured the distance between the subcortical stimulation sites and the tractography result. Positive predictive rate of the delineated tracts was assessed by comparison of subcortical IES motor function (upper extremity, lower extremity, face) with the connection of the tractography pathway in the motor cortex.

Results: We obtained 21 cortical and 8 subcortical IES sites from intraoperative mapping of motor pathways. Probabilistic q-ball had the best sensitivity (79%) as determined from cortical IES compared to deterministic q-ball (50%), probabilistic DTI (36%), and deterministic DTI (10%). The sensitivity using the q-ball algorithm (65%) was significantly higher than using DTI (23%) (p < 0.001) and the probabilistic algorithms (58%) were more sensitive than deterministic approaches (30%) (p = 0.003). Probabilistic q-ball fiber tracks had the smallest offset to the subcortical stimulation sites. The offsets between diffusion fiber tracks and subcortical IES sites were increased significantly for those cases where the diffusion fiber tracks were visibly thinner than expected. There was perfect concordance between the subcortical IES function (e.g. hand stimulation) and the cortical connection of the nearest diffusion fiber track (e.g. upper extremity cortex).

Discussion: This study highlights the tremendous utility of intraoperative stimulation sites to provide a gold standard from which to evaluate diffusion MRI fiber tracking methods and has provided an object standard for evaluation of different diffusion models and approaches to fiber tracking. The probabilistic q-ball fiber tractography was significantly better than DTI methods in terms of sensitivity and accuracy of the course through the white matter. The commonly used DTI fiber tracking approach was shown to have very poor sensitivity (as low as 10% for deterministic DTI fiber tracking) for delineation of the lateral aspects of the corticospinal tract in our study. Effects of the tumor/edema resulted in significantly larger offsets between the subcortical IES and the preoperative fiber tracks. The provided data show that probabilistic HARDI tractography is the most objective and reproducible analysis but given the small sample and number of stimulation points a generalization about our results should be given with caution. Indeed our results inform the capabilities of preoperative diffusion fiber tracking and indicate that such data should be used carefully when making pre-surgical and intra-operative management decisions.

No MeSH data available.


Related in: MedlinePlus

High positive predictive rate of the delineated fiber tracks: the closest motor tracks to the stimulation points were found to reach the cortex, where the part of the motor homunculus is known to be located. The median offset between the subcortical stimulation site and the edge of the probabilistic q-ball fiber track, found for the upper extremity (CST hand = corticospinal tract for the hand) seeding from the cerebral peduncle to the cortical IES for the hand motor, was as low as 5.5 mm.
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f0010: High positive predictive rate of the delineated fiber tracks: the closest motor tracks to the stimulation points were found to reach the cortex, where the part of the motor homunculus is known to be located. The median offset between the subcortical stimulation site and the edge of the probabilistic q-ball fiber track, found for the upper extremity (CST hand = corticospinal tract for the hand) seeding from the cerebral peduncle to the cortical IES for the hand motor, was as low as 5.5 mm.

Mentions: For example, all leg and foot subcortical stimulations were closest to delineated fiber tracts that connected with the lower extremity portion of the motor cortex, all arm and hand stimulations were closest to delineated tracts connecting the upper extremity portion of the cortex (Fig. 2), and the face subcortical stimulation was closest to a delineated tract that connected with the face motor cortical area, based on the known anatomical location of these areas of the motor homunculus in the human brain.


Quantifying diffusion MRI tractography of the corticospinal tract in brain tumors with deterministic and probabilistic methods.

Bucci M, Mandelli ML, Berman JI, Amirbekian B, Nguyen C, Berger MS, Henry RG - Neuroimage Clin (2013)

High positive predictive rate of the delineated fiber tracks: the closest motor tracks to the stimulation points were found to reach the cortex, where the part of the motor homunculus is known to be located. The median offset between the subcortical stimulation site and the edge of the probabilistic q-ball fiber track, found for the upper extremity (CST hand = corticospinal tract for the hand) seeding from the cerebral peduncle to the cortical IES for the hand motor, was as low as 5.5 mm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3815019&req=5

f0010: High positive predictive rate of the delineated fiber tracks: the closest motor tracks to the stimulation points were found to reach the cortex, where the part of the motor homunculus is known to be located. The median offset between the subcortical stimulation site and the edge of the probabilistic q-ball fiber track, found for the upper extremity (CST hand = corticospinal tract for the hand) seeding from the cerebral peduncle to the cortical IES for the hand motor, was as low as 5.5 mm.
Mentions: For example, all leg and foot subcortical stimulations were closest to delineated fiber tracts that connected with the lower extremity portion of the motor cortex, all arm and hand stimulations were closest to delineated tracts connecting the upper extremity portion of the cortex (Fig. 2), and the face subcortical stimulation was closest to a delineated tract that connected with the face motor cortical area, based on the known anatomical location of these areas of the motor homunculus in the human brain.

Bottom Line: The probabilistic q-ball fiber tractography was significantly better than DTI methods in terms of sensitivity and accuracy of the course through the white matter.The provided data show that probabilistic HARDI tractography is the most objective and reproducible analysis but given the small sample and number of stimulation points a generalization about our results should be given with caution.Indeed our results inform the capabilities of preoperative diffusion fiber tracking and indicate that such data should be used carefully when making pre-surgical and intra-operative management decisions.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, University of California, San Francisco, CA, USA.

ABSTRACT

Introduction: Diffusion MRI tractography has been increasingly used to delineate white matter pathways in vivo for which the leading clinical application is presurgical mapping of eloquent regions. However, there is rare opportunity to quantify the accuracy or sensitivity of these approaches to delineate white matter fiber pathways in vivo due to the lack of a gold standard. Intraoperative electrical stimulation (IES) provides a gold standard for the location and existence of functional motor pathways that can be used to determine the accuracy and sensitivity of fiber tracking algorithms. In this study we used intraoperative stimulation from brain tumor patients as a gold standard to estimate the sensitivity and accuracy of diffusion tensor MRI (DTI) and q-ball models of diffusion with deterministic and probabilistic fiber tracking algorithms for delineation of motor pathways.

Methods: We used preoperative high angular resolution diffusion MRI (HARDI) data (55 directions, b = 2000 s/mm(2)) acquired in a clinically feasible time frame from 12 patients who underwent a craniotomy for resection of a cerebral glioma. The corticospinal fiber tracts were delineated with DTI and q-ball models using deterministic and probabilistic algorithms. We used cortical and white matter IES sites as a gold standard for the presence and location of functional motor pathways. Sensitivity was defined as the true positive rate of delineating fiber pathways based on cortical IES stimulation sites. For accuracy and precision of the course of the fiber tracts, we measured the distance between the subcortical stimulation sites and the tractography result. Positive predictive rate of the delineated tracts was assessed by comparison of subcortical IES motor function (upper extremity, lower extremity, face) with the connection of the tractography pathway in the motor cortex.

Results: We obtained 21 cortical and 8 subcortical IES sites from intraoperative mapping of motor pathways. Probabilistic q-ball had the best sensitivity (79%) as determined from cortical IES compared to deterministic q-ball (50%), probabilistic DTI (36%), and deterministic DTI (10%). The sensitivity using the q-ball algorithm (65%) was significantly higher than using DTI (23%) (p < 0.001) and the probabilistic algorithms (58%) were more sensitive than deterministic approaches (30%) (p = 0.003). Probabilistic q-ball fiber tracks had the smallest offset to the subcortical stimulation sites. The offsets between diffusion fiber tracks and subcortical IES sites were increased significantly for those cases where the diffusion fiber tracks were visibly thinner than expected. There was perfect concordance between the subcortical IES function (e.g. hand stimulation) and the cortical connection of the nearest diffusion fiber track (e.g. upper extremity cortex).

Discussion: This study highlights the tremendous utility of intraoperative stimulation sites to provide a gold standard from which to evaluate diffusion MRI fiber tracking methods and has provided an object standard for evaluation of different diffusion models and approaches to fiber tracking. The probabilistic q-ball fiber tractography was significantly better than DTI methods in terms of sensitivity and accuracy of the course through the white matter. The commonly used DTI fiber tracking approach was shown to have very poor sensitivity (as low as 10% for deterministic DTI fiber tracking) for delineation of the lateral aspects of the corticospinal tract in our study. Effects of the tumor/edema resulted in significantly larger offsets between the subcortical IES and the preoperative fiber tracks. The provided data show that probabilistic HARDI tractography is the most objective and reproducible analysis but given the small sample and number of stimulation points a generalization about our results should be given with caution. Indeed our results inform the capabilities of preoperative diffusion fiber tracking and indicate that such data should be used carefully when making pre-surgical and intra-operative management decisions.

No MeSH data available.


Related in: MedlinePlus