The Dangers of Magnetic Resonance Imaging Diffusion Tensor Tractography in Brain Surgery

The Dangers of Magnetic Resonance Imaging Diffusion Tensor Tractography in Brain Surgery

Perspectives Commentary on: Magnetic Resonance Imaging Diffusion Tensor Tractography: Evaluation of Anatomic Accuracy of Different Fiber Tracking Soft...

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Perspectives Commentary on: Magnetic Resonance Imaging Diffusion Tensor Tractography: Evaluation of Anatomic Accuracy of Different Fiber Tracking Software Packages by Feigl et al. pp. 144-150.

Hugues Duffau, M.D., Ph.D. Professor and Chairman Department of Neurosurgery Hôpital Gui de Chauliac

The Dangers of Magnetic Resonance Imaging Diffusion Tensor Tractography in Brain Surgery Hugues Duffau

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he emerging philosophy in brain surgery, especially for cerebral tumors, is to improve both the extent of resection (and thus the overall survival) as well as the quality of life in order to move toward a functional neuro-oncology (10, 15). In this setting, neurosurgeons need to take advantage of mapping methods to create individualized maps and management plans. Surprisingly, although interindividual anatomofunctional variability was extensively studied at the cortical level using dissection in cadavers (26), functional neuroimaging (29), and intrasurgical electrical mapping (25), the white matter pathways have received less attention. Recent advances in diffusion tensor imaging (DTI) opened the door to a better understanding of the subcortical connectivity underlying brain processing (4). This technique was also applied to the noninvasive preplanning for cerebral surgery, and to the concept of multimodal navigation into the operative theater (24). However, despite a rapid development of this method in routine practice, one should be aware of the fact that DTI is not reliable enough to be the basis of any decisions in neurosurgery, and thus may be a source of danger. Indeed, in this issue of WORLD NEUROSURGERY, Feigl et al. (16) demonstrate that by comparing different fiber tracking software packages, there is a statistically significant difference in the anatomical accuracy of the tested DTI programs. On the basis of these very important results, they conclude that incorrectly displayed fibers could lead to wrong conclusions in the field of neuroscience, and could also lead to surgical decisions potentially harmful for the patient.

Key words Anatomical accuracy - Brain mapping - DTI - Navigation - Surgery -

Abbreviations and Acronyms DTI: Diffusion tensor imaging MRI: Magnetic resonance imaging

This is a crucial message for both scientists and neurosurgeons, who seem to forget that DTI is not a direct tool of visualization of the actual anatomy of fibers, but only an indirect reconstruction based on measuring the diffusion of water molecules. In fact, as reminded by Feigl et al., DTI results depend on 1) the acquisition of data (which themselves can vary by using different parameter settings for the scan sequences and by using scanners with different field strengths), 2) biomathematical models (e.g., deterministic vs. probabilistic fiber tracking), 3) the software programs (16). In this state of mind, it is interesting to note that Bu¨rgel et al. have already shown that fiber tracking with distinct software tools resulted in a clear diversity in anatomical (3). Beyond algorithms, DTI reconstruction is also dependent on the physician who decides where to put the regions of interest. For instance, it is in essence impossible to build the middle longitudinal fascicle if this pathway is not voluntarily tracked, because little is known (23). Therefore, its fibers will be wrongly incorporated within the superior longitudinal fascicle or the inferior fronto-occipital fascicle, with false results provided to the surgeon. Furthermore, when dealing with an abnormal or distorted fiber tract anatomy, in particular in brain tumors, the risk of erroneous DTI results is increased because diffusion properties may be affected by the lesion. By using neuronavigation and subcortical white matter stimulation in tumor patients, Kinoshita et al. showed that although they were able to visualize the pyramidal tract with DTI, the images failed to present the actual size of the fiber bundles (18).

Department of Neurosurgery, Gui de Chauliac Hospital, Montpellier University Medical Center; and the National Institute for Health and Medical Research (INSERM), U1051 Laboratory, Team “Brain Plasticity, Stem Cells and Glial Tumors,” Institute for Neurosciences of Montpellier, Montpellier University Medical Center, Montpellier, France To whom correspondence should be addressed: Hugues Duffau, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014) 81, 1:56-58. http://dx.doi.org/10.1016/j.wneu.2013.01.116

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PERSPECTIVES

Beyond these methodological limitations of DTI, a conceptual issue is that DTI should not be considered a tool of functional mapping, but only a tool allowing an indirect study of fiber anatomy. Indeed, in addition to the inability to reconstruct crossing and kissing fibers belonging to distinct functional subnetworks, it is still very difficult to perform a tracking of these fibers to their cortical terminations (19). This is a serious deficiency because it means that DTI is unable to give insight into the complete corticosubcortical circuits. By definition, it therefore cannot provide functional information, which depends on the understanding of synchronization of eloquent cortical epicenters connected through white matter pathways. In other words, in a hodotopical workframe of cerebral processing, i.e., organized in parallel, dynamic, and interactive large-scale distributed networks, the comprehension of brain function implies a holistic view based on the study of both cortex and subcortical connectivity (5). Therefore, DTI by itself cannot provide reliable data regarding the eloquence of a specific tract.

to its actual lack of sensitivity) and/or due to the brain shift increasing throughout the resection of voluminous tumor (thus decreasing the reliability of DTI data integrated in neuronavigation), the dogmatic rule that emerged because of the poor accuracy of neuroimaging techniques is to take 5 to 10 mm of margin around the presumed functional regions (for a review, see Gil-Robles et al. [17]). Such a strategy is against the oncological goal, that is, to optimize the extent of resection. Indeed, it was shown in more than 100 consecutive patients with diffuse low-grade gliomas in language areas that the resection could be pursued with no margin without increasing the permanent morbidity (9, 17). Finally, a recent study that aimed to assess the utility of DTI in the surgical treatment of motor eloquent tumors demonstrated that tractography of pyramidal pathways did not influence the surgical planning or the intraoperative course (2). In summary, there is a double risk of DTI, 1) to not select a patient for surgery while the tumor was actually operable, or 2) to stop the resection prematurely, with a lower impact on the natural history of the disease.

This explains discrepancies when correlating preoperative DTI and direct intraoperative electrostimulation in awake patients [the sole current tool allowing the identification of crucial structures at both cortical and subcortical levels (13)], especially concerning cognitive functions such as language. For example, a recent series demonstrated a good correspondence between both techniques in only 82% of cases, showing that DTI was not yet optimal for mapping language tracts. It means that negative tractography does not rule out the persistence of a fiber tract, especially when invaded by a glioma (20).

Last but not least, the risk for young neurosurgeons who use DTI regularly in the operating theater (DTI incorporated into the neuronavigational system or acquired in real time with intrasurgical magnetic resonance imaging [MRI]) is becoming dependent on neuroimaging. The danger is for them to not learn optimally the functional anatomy of the brain (by combining anatomic dissection, intraoperative electrical mapping, and models of cognitive neuroscience) and thus to not be able to operate in the central nervous system without any intrasurgical neuroimaging, on the sole basis of their own mental imaging validated by online feedback provided by electrophysiology (14). Indeed, it is worth noting that so far, no series in the literature based on DTI reported that image-guided surgery was able to increase simultaneously 1) the indications of surgery in eloquent areas, 2) the extent of resection, and 3) the quality of life. Interestingly, a recent meta-analysis studying 8091 patients (from 90 series published between 1990 and 2010) who underwent surgical resection for a brain glioma has demonstrated that the use of intrasurgical electrical mapping allowed a statistically significant reduction of permanent deficit, despite an increased rate of resection within eloquent areas, and despite an increase of the extent of resection (6). These unique results show that intraoperative electrical stimulation remains the goal standard in brain surgery, especially at the subcortical level. Therefore, DTI needs to be validated by intraoperative electrophysiological techniques before it can be used routinely for surgical practice. Correlations between DTI and anatomic dissection using the Klinger technique may also participate in this validation of MRI tensor diffusion tractography (22, 28). In conclusion, DTI currently must be considered a research tool in the field of cognitive neurosciences, and neurosurgeons should be aware of the dangers of DTI before applying tractography results both for preplanning and in the operating room.

Consequently, several negative impacts of DTI should be underlined in neurosurgical practice. The first limitation is that brain (tumor) surgery could not be proposed because DTI showed fibers a priori considered as critical very near or within the tumor, whereas it was in fact possible to remove it with no permanent deficit—thus with a loss of chance from an oncological point of view, because surgical resection will not be performed. This point is particularly true for diffuse low-grade gliomas invading eloquent cortex, such as the so-called rolandic area, Broca area or Wernicke area (1, 7, 27). Indeed, due to mechanisms of cortical plasticity elicited by the slow growth of the lesion, the fibers connected to these sites (which have been compensated by the recruitment of other cortical regions) are not critical anymore and can be cut with no irrevocable neurological worsening, even if they are anatomically part of a functional pathway, such as the left inferior longitudinal fascicle or left uncinate fascicle (11, 12, 21). Therefore, the glioma was actually resectable with a favorable outcome, although these regions were thought to be crucial on the basis of DTI. Of course, in these patients, it is mandatory to perform an awake procedure with intraoperative cortical and subcortical stimulation mapping to check the absence of eloquence of these structures invaded by the glioma (8, 9). Moreover, intraoperatively, beyond the risk of damaging eloquent structures not detected by DTI (due

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Citation: World Neurosurg. (2014) 81, 1:56-58. http://dx.doi.org/10.1016/j.wneu.2013.01.116 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.

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