Acta Neurochir DOI 10.1007/s00701-015-2411-y
CLINICAL ARTICLE - BRAIN TUMORS
Feasibility of diffusion tensor tractography for preoperative prediction of the location of the facial and vestibulocochlear nerves in relation to vestibular schwannoma Masanori Yoshino 1 & Taichi Kin 1 & Akihiro Ito 1 & Toki Saito 2 & Daichi Nakagawa 1 & Kenji Ino 4 & Kyousuke Kamada 3 & Harushi Mori 4 & Akira Kunimatsu 4 & Hirofumi Nakatomi 1 & Hiroshi Oyama 2 & Nobuhito Saito 1
Received: 16 December 2014 / Accepted: 23 March 2015 # Springer-Verlag Wien 2015
Abstract Background According to recent findings, diffusion tensor tractography (DTT) only allows prediction of facial nerve location in relation to vestibular schwannoma (VS) with high probability. However, previous studies have not mentioned why only the facial nerve was selectively visualized. Our previous report investigated the optimal conditions of DTT for normal facial and vestibulocochlear nerves. In the present study, we applied the optimal conditions of DTT to VS patients to assess the feasibility of DTT for the facial and vestibulocochlear nerves. Methods We investigated 11 patients with VS who underwent tumor resection. Visualized tracts were compared with locations of the facial and cochlear nerves as identified by intraoperative electrophysiological monitoring. Results With the proposed method, visualized tracts corresponded to pathway area of the facial or cochlear nerves in nine of 11 patients (81.8 %); specifically, to the pathway area of the facial nerve in three of 11 patients (27.3 %), and to
* Masanori Yoshino [email protected] 1
2
Department of Neurosurgery, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan Departments of Clinical Information Engineering, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan
3
Department of Neurosurgery, Asahikawa Medical University, 2-1 Midorigaoka-Higashi, Asahikawa, Hokkaido 078-8510, Japan
4
Departments of Radiology, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan
the pathway area of the cochlear nerve in six of 11 patients (54.5 %). Conclusions We visualized facial or vestibulocochlear nerves in nine of 11 patients (81.8 %). For the first time, DTT proved able to visualize not only the facial nerve but also the vestibulocochlear nerve in VS patients. Despite our findings, good methods for distinguishing whether a visualized nerve tract represents facial nerve, vestibulocochlear nerve, or only noise remain unavailable. Close attention should therefore be paid to the interpretation of visualized fibers. Keywords Diffusion tensor tractography . Facial nerve . Vestibulocochlear nerve . Vestibular schwannoma . Fractional anisotropy threshold
Abbreviations DTT Diffusion tensor tractography ESEElicited dorsal cochlear nucleus action DNAP potential FA Fractional anisotropy ROI Region of interest VS Vestibular schwannoma
Introduction The final objective of surgery to remove vestibular schwannoma (VS) is to excise the tumor as thoroughly as possible while preserving the functions of the facial and cochlear nerves as fully as possible [11]. In recent years, advances in diagnostic preoperative imaging have contributed to improved rates of postoperative preservation of these
Acta Neurochir
functions [7, 8, 13]. Most recently, preoperative prediction of the locations of the nerves using diffusion tensor tractography (DTT) has been adopted as an aid to improving preservation rates for facial nerve function. Taoka et al. were the first to report the application of DTT to VS, and were able to visualize fiber tracts that coincided with the facial nerve in five of eight patients (62.5 %) [14]. Three other groups subsequently applied DTT to VS for preoperative prediction of nerve locations [1, 3, 10]. Gerganov et al. reported agreement between the visualized fiber tract and facial nerve locations in 20 of 22 patients (90.9 %) with VS (mean size, 27 mm) [3]. Although the facial nerve has been visualized in VS patients, none of those reports mentioned the reasons why only the facial nerve was visualized selectively even though other structures (such as the vestibulocochlear nerve, noise, and tumor itself) could be visualized theoretically. In a previous report, we investigated the appropriate conditions for performing DTT for normal facial and vestibulocochlear nerves [15]. The present study examined whether DTT could visualize not only the facial nerve but also the vestibulocochlear nerve in VS patients using the same conditions for fiber tracking as employed in the earlier study of normal subjects.
Image acquisition
Materials and methods
Setting of seed ROIs and FA thresholds
Patient population
We used the methods described below to set the seed ROIs and FA thresholds in the same manner as in our earlier study of normal facial and vestibulocochlear nerves [15].
We investigated 11 patients (six males, five females) with VS who underwent both DTT as a preoperative examination and tumor resection, and for whom facial and cochlear nerve locations were definitively identified by intraoperative electrophysiological monitoring. Mean age was 40.0 years (range, 18–58 years). Preoperative facial nerve function was House & Brackmann Classification grade I in all patients [4]. Preoperative hearing function was graded using the Gardner-Robertson Classification [2]: grade 1 in five patients; grade 2 in one patient; grade 3 in two patients; grade 4 in 0 patients; and grade 5 in three patients. Tumor size was measured in axial cross section as the largest diameter parallel to the posterior surface of the petrous bone. Mean size was 29.7 mm (range, 20.1–40.4 mm). In addition, determination of the origin of the VS during the surgery revealed the superior vestibular nerve in three patients (27.2 %) and the inferior vestibular nerve in eight patients (72.7 %) (Table 1). The internal review board of the University of Tokyo Hospital approved the study protocol, and written informed co nsen t w as o btaine d fro m all su bjec ts prior to participation.
MRI was performed using a 3.0-T system (Signa 3.0 T; GE, Milwaukee, WI, USA) equipped with an eight-channel phased-array head coil. DT images were obtained with a single-shot spin-echo echo-planar sequence using the following protocol: repetition time, 17,000 ms; echo time, 65.6 ms; slice thickness, 2.5 mm with no gap; field of view, 25.6 cm; number of excitations, 1; matrix size, 128×128; and reconstructed images zero-fill interpolated to 256×256. DT imaging data were acquired along 30 non-collinear gradient directions with a b-value of 1000 s/mm2, with an additional zero bimage (B0 image). Realignment of these images and compensation for eddy-current morphing were performed on the basis of the B0 image on a workstation equipped with the MR unit. DTI data were transferred to a personal computer (Precision T7500; Dell, Round Rock, TX; CPU: Intel Xeon X5550, 2.67 GHz, 2.66 GHz; PAM: 8.00 GB; graphics card: NVIDIA Quadro FX5800). DTT was performed using dTV-II SR [6]. We used ROIs as seed points (seed ROIs) and FA thresholds for fiber tracking. A target ROI was not used. As for other parameters such as step length and turning angle, we used default values of dTV (step length, 160 mm; turning angle, 30°). Interpolation along the z-axis was also applied to obtain isotropic data (voxel size, 0.9×0.9×0.9 cm).
Setting of seed ROIs To include all nerves coursing inside the internal auditory canal, seed ROIs were placed at the porus of the internal auditory canal in a plane perpendicular to the courses of the facial and vestibulocochlear nerves (Fig. 1a). At the time of setting seed ROIs, the internal auditory canal was comprehensively surrounded by manually drawing a line at the outer edge of the internal auditory canal, while each case was determined separately to minimize inclusion of surrounding tissues as much as possible (Fig. 1b). All these procedures were performed on the basis of B0 images, but for cases in which identification of the internal auditory canal was difficult, identification was performed using a map of the suitable apparent diffusion coefficient. Setting of FA thresholds The FA threshold was set at a variable value. The variable FA threshold for each patient was increased in increments of 0.01,
Acta Neurochir Table 1
Patient demographic and clinical characteristics
Patient
Age/sex
Size (mm)
Origin of tumor
Preoperative hearing function
Preoperative facial nerve function
Postoperative hearing function
Postoperative facial nerve function
1 2 3 4
34, M 52, F 41, M 50, M
31.5 20.9 28.8 39.6
IVN IVN IVN IVN
1 1 3 2
I I I I
1 1 4 5
I I I II
5 6 7 8 9 10 11
18, F 36, F 34, F 30, M 58, M 38, F 49, M
40.4 32.0 27.0 28.3 36.5 22.1 20.1
IVN IVN SVN IVN SVN SVN IVN
1 5 1 3 5 1 5
I I I I I I I
5 5 1 3 5 1 5
I II II I I I II
M male, F female, SVN superior vestibular nerve, IVN inferior vestibular nerve
with the upper limit being the level just before fiber tracts disappeared. Verification of fiber tracts visualized by DTT From among the visualized fiber tracts, we verified as true fiber tracts those that ran on the surface or inside of the tumor and reached the brainstem and were identified as nerves based on electrophysiological testing performed during the operation. That is, for fiber tracts visualized by DTT and facial and cochlear nerves identified by electrophysiological testing, paths in the central portion of the cistern were classified, on the basis of the report of Sampath et al. [12], as coursing superior, anterior, inferior, posterior or inside the tumor. In addition, anterior and posterior fiber tracts were classified as superior one-third, middle one-third, or inferior one-third. In cases where there was agreement between the pathway area of a fiber tract visualized by DTT and the pathway area of a nerve identified Fig. 1 Method for setting the seed region of interest (ROI). In the proposed method, the porus of the internal auditory canal is viewed from a direction parallel to the courses of the nerves inside the internal auditory canal (a arrow), and the seed ROI is placed at the porus of the internal auditory canal in a plane perpendicular to the courses of the nerves (b red circle)
during surgery, visualization of the nerve by DTT was judged as correct. Identifying the vestibular nerve electrophysiologically during surgery is not currently possible. We therefore judged visualized fiber tracts that coincided with the cochlear nerve identified during surgery as the vestibulocochlear nerve. Regarding identification methods for nerves, the facial nerve was identified by the presence of facial muscle action potentials elicited by direct facial nerve fascicle stimulation at 0.1–0.2 mA. With regard to the cochlear nerve, since we invented electric stimuli-elicited dorsal cochlear nucleus action potential (ESE-DNAP) monitoring [5, 9], we could identify the specific direct connection of the specific nerve fascicle with the dorsal cochlear nucleus by intraoperative electrical stimulation around 0.2–0.4 mA. Intraoperative identification of nerves was performed by the neurosurgeon who performed the surgery (H.N.). DTT visualization was performed by the first author (M.Y.), and consistency with the intraoperative findings was judged by consultation
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between a neurosurgeon (T.K.) who played no part in the surgery or preoperative DTT visualization and the first author (M.Y.).
Table 2 Prediction of nerves by diffusion tensor tractography when using variable values for the fractional anisotropy threshold and actual intraoperative findings Patient
Results Outcomes for facial nerve and hearing functions Postoperative facial nerve function according to House & Brackmann Classification was grade I in seven patients, grade II in four patients [4]. That is, all patients achieved House & Brackmann Classification grade I–III (100 %). Postoperative hearing function was graded using the Gardner-Robertson Classification [2], and was grade 1 in four patients, grade 2 in 0 patients, grade 3 in one patient, grade 4 in one patient, and grade 5 in five patients. Functional hearing (50 % speech discrimination score) was preserved in five of eight patients (62.5 %) (Table 1). Intraoperative locations of the facial and cochlear nerves in relation to VS We identified facial nerve location in all patients based on the presence of facial muscle action potentials elicited by direct stimulation of facial nerve fascicles. The facial nerve was located on the superior tumor surface in one patient, on the anterosuperior one-third of the tumor surface in seven patients, and on the anterior middle one-third of the tumor surface in three patients. We also identified cochlear nerve location in 11 patients based on the presence of ESE-DNAP elicited by direct stimulation of cochlear nerve fascicles. The cochlear nerve was located on the anteroinferior one-third of the tumor surface in seven patients, on the inferior tumor surface in three patients, and on the posterior middle one-third of the tumor surface in one patient (Table 2). Prediction by DTT and verification of prediction results Fiber tracts running from the internal auditory canal to the brainstem were visualized in ten patients. When we verified the visualized fiber tracts with the true nerves identified intraoperatively, we found agreement between the pathway area of visualized fiber tracts and the pathway area of the facial or cochlear nerves identified during surgery in nine of these ten patients. More specifically, in three of the ten patients (30 %) in whom fiber tracts were visualized, the visualized fiber tract corresponded to the pathway area of the facial nerve, and this corresponded to the pathway area of the cochlear nerve in six patients (60 %). For all 11 patients, the visualized fiber tracts corresponded to the pathway area of the facial or cochlear nerve in nine patients (81.8 %), to the pathway area of the facial nerve in three patients (27.3 %), and to the pathway area of the cochlear nerve in six patients (54.5 %) (Table 2).
Intraoperative finding
DTT outcome
Facial nerve
Cochlear nerve
1 2 3 4 5 6
AS S AS AM AS AS
AI PM AI I AI AI
AI,PI PM AI I AS,I -
7 8 9 10 11
AM AS AS AM AS
AI AI I I AI
I AS I I AS
Courses of fibers in the central portion of the cistern were classified into nine areas: S superior to the tumor; AS anterior superior one-third; AM anterior middle one-third; AI anterior inferior one-third; I inferior; PI posterior inferior one-third; PM posterior middle one-third; and PS posterior superior one-third; - not visualized
Representative cases Case 2 The patient was a 52-year-old woman who presented with hearing loss and right VS (Fig. 2a). The tumor was 20.9 mm in diameter. When FA thresholds were set at the upper limit, a fiber tract was visualized in the posterior middle one-third to the tumor (Fig. 2b–d). Surgery was performed using a lateral suboccipital approach. Electrophysiological diagnosis performed during surgery confirmed that the facial nerve ran superior to the tumor, while the cochlear nerve ran in the posterior middle one-third compared to the tumor (Fig. 2e and f). These results show that the pathway area of the visualized fiber tract corresponded with the actual pathway area of the cochlear nerve. In this patient, we intended to preserve hearing function, and therefore only performed a biopsy at that time, since resection of the tumor without injury to the cochlear nerve using a lateral suboccipital approach seemed very difficult. We subsequently performed complete resection of the tumor using an extended middle cranial fossa approach.
Case 8 The patient was a 30-year-old man who presented with hearing loss and right VS (Fig. 3a). The tumor was 28.3 mm in maximum diameter. When FA thresholds were set at the upper
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Fig. 2 Case 2. Contrast-enhanced fast imaging employing steady-state acquisition imaging shows left cerebellopontine angle vestibular schwannoma in the (a) axial view. b Axial view of diffusion tensor tractography (DTT). c Sagittal view of DTT. d Oblique view of DTT. DTT when using the upper limit of the FA threshold visualizes the fiber tract running in the posterior middle one-third to the tumor. e, f
Fig. 3 Case 8. Contrastenhanced fast imaging employing steady-state acquisition imaging showing left cerebellopontine angle vestibular schwannoma in the a axial view. b Axial view of diffusion tensor tractography (DTT). c Sagittal view of DTT. DTT when using the upper limit of the fractional anisotropy threshold visualizes the fiber tract running in the anterior superior one-third to the tumor. d Intraoperative view. Electrophysiological diagnosis performed during the surgery confirms that the facial nerve runs in the anterior superior onethird to the tumor (asterisk)
Intraoperative view. Electrophysiological diagnosis performed during the surgery confirms that the cochlear nerve passes in the posterior middle one-third to the tumor (f asterisk). Positive wave of elicited dorsal cochlear nucleus action potential (ESE-DNAP) represents the presence of the cochlear nerve (e arrowhead)
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limit, fiber tracts were visualized that ran anterior superior one-third to the tumor (Fig. 3b and c). Surgery was performed by a lateral suboccipital approach. Electrophysiological diagnosis performed during the surgery confirmed that the facial nerve ran in the anterosuperior onethird to the tumor (Fig. 3d), while the cochlear nerve passed in the anteroinferior one-third to the tumor. These results showed that the pathway area of the visualized fiber tract corresponded with the actual pathway area of the facial nerve.
Discussion In this report, we indicated for the first time that DTT allows visualization of not only the facial nerve but also the vestibulocochlear nerve in VS patients. Despite these findings, predicting whether a visualized tract represents the facial nerve, vestibulocochlear nerve, or mere noise prior to surgery is still difficult. In fact, we were uncertain whether the fiber tract visualized on DTT represented facial nerve, vestibulocochlear nerve, or mere noise in case 2, because the visualized fiber tract followed a course that the facial and vestibulocochlear nerves were considered unlikely to take [12]. The next step is therefore to develop a good method to distinguish whether a visualized tract represents facial nerve, vestibulocochlear nerve, or mere noise prior to surgery; until then, we cannot use DTT for preoperative prediction of nerve locations in relation to VS with confidence.
Comparison with results from previous reports Application of DTT to VS was first reported by Taoka et al. [14], and in a later study the preoperative visualization rate for the facial nerve was increased to 90.9 % [3]. On the other hand, visualization of the vestibulocochlear nerve was either not mentioned [1, 10] or was reported as impossible [3]. The present results are thus very different (Table 3). Three reasons can be considered for the large differences between our results and those of earlier studies. The chief reason can be surmised to be that this study set the FA threshold at the upper limit in each patient. Other possible reasons are problems with interpretation of visualized fiber tracts, and differences in the imaging equipment, imaging conditions, and software used. With regard to interpretation, as shown in this study, completely eliminating false tracts is difficult, and even if only nerve fiber tracts can be visualized, distinguishing whether a depicted fiber represents facial or vestibulocochlear nerve or noise is also problematic. As a result, even though fibers other than the facial nerve may have been visualized, previous reports have judged the visualized fiber as representing the facial nerve, thus increasing the visualization rate for the facial nerve. In particular, in cases where the cochlear and facial nerves run in parallel, errors in judgment may be made, and caution in this regard is necessary. With regard to differences in equipment and conditions, it will be necessary in the future to validate the methods described in this study by applying the same imaging conditions and software. Limitations of this study
Capacity of DTT to visualize the facial and vestibulocochlear nerves The visualized fiber tract in six patients (6/11; 54.5 %) in whom fiber tracts were visualized corresponded to the pathway area of the cochlear nerve, while in three patients (27.3 %) it corresponded to the pathway area of the facial nerve. Thus, in this study, the visualization rate was higher for the vestibulocochlear nerve than for the facial nerve. The reason for this might be that this study set the FA threshold at the upper limit for each patient. This means that nerve fiber tracts with higher FA values can be visualized at a higher rate than those with lower FA values. In addition, when we applied DTT for VS patients, the nerve fiber tract visualized by DTT as the vestibulocochlear nerve presumably included both the remnant normal vestibular nerve and the cochlear nerve, since the cochlear nerve is inseparable from the vestibular nerve at the brainstem and cerebellopontine segments. As a result, FA values of the nerve fiber tract visualized as the vestibulocochlear nerve were higher than those of the facial nerve, leading to a higher rate of vestibulocochlear nerve visualization by DTT.
In this study, the upper limit of the FA threshold was set for each patient. As a result, the facial or vestibulocochlear nerve was visualized in nine of 11 VS patients. However, increasing the FA threshold and setting the upper limit decreased not only the noise but also the visualization of actual nerve fiber tracts. We cannot rule out the possibility that this led to a decrease in the predictive value for the facial nerve compared with earlier reports. Another problem is the current visualization capacity of DTT. We still have no good method for distinguishing in advance whether a visualized fiber represents facial nerve, vestibulocochlear nerve, or simply noise, which would decrease the reliability of DTT for preoperative prediction of nerve location. The present results revealed that the fibers visualized when the FA threshold is at the upper limit show a strong tendency to coincide with the course of the vestibulocochlear nerve. The results of this study may contribute to the development of methods for distinguishing the vestibulocochlear nerve from the facial nerve and noise, and further studies of a greater number of cases are warranted. Imaging conditions for DTT also need to be investigated further.
Visualization rate of cochlear nerve (%)
Not mentioned
Not verified
0.0
Not mentioned
66.6
Visualization rate of facial nerve (%)
62.5
Not verified
90.9
100
25.5
Seed ROI
Placement at the fundus of the internal auditory meatus on the sagittal cross section Placement at the intracanalicular compartment for the facial/ vestibular complex Placement to the internal auditory meatus Placement at around the circumference of the tumor in a midcisternal portion on the sagittal cross section Placement at the porus of the internal auditory meatus on a plane perpendicular to the facial and vestibulocochlear nerves
Conclusions In this study, DTT was proved to be able to visualize not only the facial nerve but also the vestibulocochlear nerve, which has been considered difficult to achieve with conventional visualization methods. Despite our findings, good methods for distinguishing whether a visualized nerve tract represents facial nerve, vestibulocochlear nerve, or noise remain unavailable. Close attention should therefore be paid to the interpretation of visualized fibers. Acknowledgments This work was supported in part by Grant-in-Aid for Challenging Exploratory Research 25670618. We wish to thank Minoru Tanaka for suggesting this investigation. Conflict of interest None.
References 1.
Upper limit for each patient
0.15
0.1
0.2
0.1
FA threshold
2. 3.
4.
DTV
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i PLAN
3D slicer
DTV
Software
5.
Vestibular schwannoma Present study
26.2 (mean)
Vestibular schwannoma Cerebellopontine angle tumor Gergnov et al. [3], 2010 Roundy et al. [10], 2012
35.8 (mean)
Vestibular schwannoma Chen et al. [1] 2007
27.0 (mean)
29 (mean) Vestibular schwannoma Taoka et al. [14], 2006
10–30 (range)
Tumor diameter (mm) Test subject
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Table 3
Comparison with earlier reports of diffusion tensor tractography for vestibular schwannoma patients
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Chen DQ, Quan J, Guha A, Tymianski M, Mikulis D, Hodaie M (2011) Three-dimensional in vivo modeling of vestibular schwannomas and surrounding cranial nerves with diffusion imaging tractography. Neurosurgery 68:1077–1083 Gardner G, Robertson J (1987) Hearing preservation in unilateral acoustic neuroma surgery. Ann Otol Rhinol Laryngol 97:55–66 Gerganov VM, Giordano M, Samii M, Samii A (2011) Diffusion tensor imaging-based fiber tracking for prediction of the position of the facial nerve in relation to large vestibular schwannomas. J Neurosurg 115:1087–1093 House JW, Brackmann DE (1985) Facial nerve grading system. Otolaryngol Head Neck Surg 93:146–147 Magnan J, Parikh B, Miyazaki H (2013) Functional Surgery of Cerebellopontine Angle by Minimally Invasive Retrosigmoid Approach. In: Miyazaki H, Nerve Monitoring for Cerebellopontine Angle Surgery. JP Medical Ltd, New Delhi, pp 19–28 Masutani Y, Aoki S, Abe O, Hayashi N, Otomo K (2003) MR diffusion tensor imaging: recent advance and new techniques for diffusion tensor visualization. Eur J Radiol 46:53–66 Mikami T, Minamida Y, Yamaki T, Koyanagi I, Nonaka T, Houkin K (2005) Cranial nerve assessment in posterior fossa tumors with fast imaging employing steady-state acquisition (FIESTA). Neurosurg Rev 28:261–266 Nakai T, Yamamoto H, Tanaka K, Koyama J, Fujita A, Taniguchi M, Hosoda K, Kohmura E (2013) Preoperative detection of the facial nerve by high-field magnetic resonance imaging in patients with vestibular schwannoma. Neuroradiology 55:615–620 Nakatomi H, Miyazaki H, Tanaka M, Kin T, Yoshino M, Oyama H, Usui M, Moriyama H, Kojima H, Kaga K, Saito N (2014) Improved preservation of function during acoustic neuroma surgery. J Neurosurg 122(1):24–33 Roundy N, Delashaw JB, Cetas JS (2012) Preoperative identification of the facial nerve in patients with large cerebellopontine angle tumors using high-density diffusion tensor imaging: Clinical article. J Neurosurg 116:697–702 Samii M, Gerganov V, Samii A (2006) Improved preservation of hearing and facial nerve function in vestibular schwannoma surgery via the retrosigmoid approach in a series of 200 patients. J Neurosurg 105:527–535
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Sampath P, Rini D, Long DM (2000) Microanatomical variations in the cerebellopontine angle associated with vestibular schwannomas (acoustic neuromas): a retrospective study of 1006 consecutive cases. J Neurosurg 92:70–78 Shigematsu Y, Korogi Y, Hirai T, Okuda T, Ikushima I, Sugahara T, Liang L, Takahashi M (1999) Contrast-enhanced CISS MRI of vestibular schwannomas: phantom and clinical studies. J Comput Assist Tomogr 23:224–231 Taoka T, Hirabayashi H, Nakagawa H, Sakamoto M, Myochin K, Hirohashi S, Iwasaki S, Sakaki T, Kichikawa K (2006) Displacement of the facial nerve course by vestibular schwannoma: preoperative visualization using diffusion tensor tractography. J Magn Reson Imaging 24:1005–1010 Yoshino M, Kin T, Ito A, Saito T, Nakagawa D, Kamada K, Mori H, Kunimatsu A, Nakatomi H, Oyama H, Saito N (2014) Diffusion tensor tractography of normal facial and vestibulocochlear nerves. Int J Comput Assist Radiol Surg. doi:10.1007/s11548-014-1129-2
Comments The authors describe a novel modification of a DTI/DTT technique to identify the cochlear nerve by increasing the fraction anisotropy (FA) threshold. While this technique decreases the ability to identify facial nerves, it has a merit in identifying the cochlear nerve, which would be of importance if a hearing-preservation surgery is planned. The identification of vestibular nerves and potential misinterpretation between the vestibular nerve and cochlear nerve is a major concern with this method. Future modification of this technique will hopefully enable us to obtain accurate identification of both facial and cochlear nerves by adjusting the FA threshold in the same setting and identifying different cranial nerve trajectory. Amir Dehdashti NY, USA
CLINICAL ARTICLE - BRAIN TUMORS
Feasibility of diffusion tensor tractography for preoperative prediction of the location of the facial and vestibulocochlear nerves in relation to vestibular schwannoma Masanori Yoshino 1 & Taichi Kin 1 & Akihiro Ito 1 & Toki Saito 2 & Daichi Nakagawa 1 & Kenji Ino 4 & Kyousuke Kamada 3 & Harushi Mori 4 & Akira Kunimatsu 4 & Hirofumi Nakatomi 1 & Hiroshi Oyama 2 & Nobuhito Saito 1
Received: 16 December 2014 / Accepted: 23 March 2015 # Springer-Verlag Wien 2015
Abstract Background According to recent findings, diffusion tensor tractography (DTT) only allows prediction of facial nerve location in relation to vestibular schwannoma (VS) with high probability. However, previous studies have not mentioned why only the facial nerve was selectively visualized. Our previous report investigated the optimal conditions of DTT for normal facial and vestibulocochlear nerves. In the present study, we applied the optimal conditions of DTT to VS patients to assess the feasibility of DTT for the facial and vestibulocochlear nerves. Methods We investigated 11 patients with VS who underwent tumor resection. Visualized tracts were compared with locations of the facial and cochlear nerves as identified by intraoperative electrophysiological monitoring. Results With the proposed method, visualized tracts corresponded to pathway area of the facial or cochlear nerves in nine of 11 patients (81.8 %); specifically, to the pathway area of the facial nerve in three of 11 patients (27.3 %), and to
* Masanori Yoshino [email protected] 1
2
Department of Neurosurgery, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan Departments of Clinical Information Engineering, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan
3
Department of Neurosurgery, Asahikawa Medical University, 2-1 Midorigaoka-Higashi, Asahikawa, Hokkaido 078-8510, Japan
4
Departments of Radiology, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan
the pathway area of the cochlear nerve in six of 11 patients (54.5 %). Conclusions We visualized facial or vestibulocochlear nerves in nine of 11 patients (81.8 %). For the first time, DTT proved able to visualize not only the facial nerve but also the vestibulocochlear nerve in VS patients. Despite our findings, good methods for distinguishing whether a visualized nerve tract represents facial nerve, vestibulocochlear nerve, or only noise remain unavailable. Close attention should therefore be paid to the interpretation of visualized fibers. Keywords Diffusion tensor tractography . Facial nerve . Vestibulocochlear nerve . Vestibular schwannoma . Fractional anisotropy threshold
Abbreviations DTT Diffusion tensor tractography ESEElicited dorsal cochlear nucleus action DNAP potential FA Fractional anisotropy ROI Region of interest VS Vestibular schwannoma
Introduction The final objective of surgery to remove vestibular schwannoma (VS) is to excise the tumor as thoroughly as possible while preserving the functions of the facial and cochlear nerves as fully as possible [11]. In recent years, advances in diagnostic preoperative imaging have contributed to improved rates of postoperative preservation of these
Acta Neurochir
functions [7, 8, 13]. Most recently, preoperative prediction of the locations of the nerves using diffusion tensor tractography (DTT) has been adopted as an aid to improving preservation rates for facial nerve function. Taoka et al. were the first to report the application of DTT to VS, and were able to visualize fiber tracts that coincided with the facial nerve in five of eight patients (62.5 %) [14]. Three other groups subsequently applied DTT to VS for preoperative prediction of nerve locations [1, 3, 10]. Gerganov et al. reported agreement between the visualized fiber tract and facial nerve locations in 20 of 22 patients (90.9 %) with VS (mean size, 27 mm) [3]. Although the facial nerve has been visualized in VS patients, none of those reports mentioned the reasons why only the facial nerve was visualized selectively even though other structures (such as the vestibulocochlear nerve, noise, and tumor itself) could be visualized theoretically. In a previous report, we investigated the appropriate conditions for performing DTT for normal facial and vestibulocochlear nerves [15]. The present study examined whether DTT could visualize not only the facial nerve but also the vestibulocochlear nerve in VS patients using the same conditions for fiber tracking as employed in the earlier study of normal subjects.
Image acquisition
Materials and methods
Setting of seed ROIs and FA thresholds
Patient population
We used the methods described below to set the seed ROIs and FA thresholds in the same manner as in our earlier study of normal facial and vestibulocochlear nerves [15].
We investigated 11 patients (six males, five females) with VS who underwent both DTT as a preoperative examination and tumor resection, and for whom facial and cochlear nerve locations were definitively identified by intraoperative electrophysiological monitoring. Mean age was 40.0 years (range, 18–58 years). Preoperative facial nerve function was House & Brackmann Classification grade I in all patients [4]. Preoperative hearing function was graded using the Gardner-Robertson Classification [2]: grade 1 in five patients; grade 2 in one patient; grade 3 in two patients; grade 4 in 0 patients; and grade 5 in three patients. Tumor size was measured in axial cross section as the largest diameter parallel to the posterior surface of the petrous bone. Mean size was 29.7 mm (range, 20.1–40.4 mm). In addition, determination of the origin of the VS during the surgery revealed the superior vestibular nerve in three patients (27.2 %) and the inferior vestibular nerve in eight patients (72.7 %) (Table 1). The internal review board of the University of Tokyo Hospital approved the study protocol, and written informed co nsen t w as o btaine d fro m all su bjec ts prior to participation.
MRI was performed using a 3.0-T system (Signa 3.0 T; GE, Milwaukee, WI, USA) equipped with an eight-channel phased-array head coil. DT images were obtained with a single-shot spin-echo echo-planar sequence using the following protocol: repetition time, 17,000 ms; echo time, 65.6 ms; slice thickness, 2.5 mm with no gap; field of view, 25.6 cm; number of excitations, 1; matrix size, 128×128; and reconstructed images zero-fill interpolated to 256×256. DT imaging data were acquired along 30 non-collinear gradient directions with a b-value of 1000 s/mm2, with an additional zero bimage (B0 image). Realignment of these images and compensation for eddy-current morphing were performed on the basis of the B0 image on a workstation equipped with the MR unit. DTI data were transferred to a personal computer (Precision T7500; Dell, Round Rock, TX; CPU: Intel Xeon X5550, 2.67 GHz, 2.66 GHz; PAM: 8.00 GB; graphics card: NVIDIA Quadro FX5800). DTT was performed using dTV-II SR [6]. We used ROIs as seed points (seed ROIs) and FA thresholds for fiber tracking. A target ROI was not used. As for other parameters such as step length and turning angle, we used default values of dTV (step length, 160 mm; turning angle, 30°). Interpolation along the z-axis was also applied to obtain isotropic data (voxel size, 0.9×0.9×0.9 cm).
Setting of seed ROIs To include all nerves coursing inside the internal auditory canal, seed ROIs were placed at the porus of the internal auditory canal in a plane perpendicular to the courses of the facial and vestibulocochlear nerves (Fig. 1a). At the time of setting seed ROIs, the internal auditory canal was comprehensively surrounded by manually drawing a line at the outer edge of the internal auditory canal, while each case was determined separately to minimize inclusion of surrounding tissues as much as possible (Fig. 1b). All these procedures were performed on the basis of B0 images, but for cases in which identification of the internal auditory canal was difficult, identification was performed using a map of the suitable apparent diffusion coefficient. Setting of FA thresholds The FA threshold was set at a variable value. The variable FA threshold for each patient was increased in increments of 0.01,
Acta Neurochir Table 1
Patient demographic and clinical characteristics
Patient
Age/sex
Size (mm)
Origin of tumor
Preoperative hearing function
Preoperative facial nerve function
Postoperative hearing function
Postoperative facial nerve function
1 2 3 4
34, M 52, F 41, M 50, M
31.5 20.9 28.8 39.6
IVN IVN IVN IVN
1 1 3 2
I I I I
1 1 4 5
I I I II
5 6 7 8 9 10 11
18, F 36, F 34, F 30, M 58, M 38, F 49, M
40.4 32.0 27.0 28.3 36.5 22.1 20.1
IVN IVN SVN IVN SVN SVN IVN
1 5 1 3 5 1 5
I I I I I I I
5 5 1 3 5 1 5
I II II I I I II
M male, F female, SVN superior vestibular nerve, IVN inferior vestibular nerve
with the upper limit being the level just before fiber tracts disappeared. Verification of fiber tracts visualized by DTT From among the visualized fiber tracts, we verified as true fiber tracts those that ran on the surface or inside of the tumor and reached the brainstem and were identified as nerves based on electrophysiological testing performed during the operation. That is, for fiber tracts visualized by DTT and facial and cochlear nerves identified by electrophysiological testing, paths in the central portion of the cistern were classified, on the basis of the report of Sampath et al. [12], as coursing superior, anterior, inferior, posterior or inside the tumor. In addition, anterior and posterior fiber tracts were classified as superior one-third, middle one-third, or inferior one-third. In cases where there was agreement between the pathway area of a fiber tract visualized by DTT and the pathway area of a nerve identified Fig. 1 Method for setting the seed region of interest (ROI). In the proposed method, the porus of the internal auditory canal is viewed from a direction parallel to the courses of the nerves inside the internal auditory canal (a arrow), and the seed ROI is placed at the porus of the internal auditory canal in a plane perpendicular to the courses of the nerves (b red circle)
during surgery, visualization of the nerve by DTT was judged as correct. Identifying the vestibular nerve electrophysiologically during surgery is not currently possible. We therefore judged visualized fiber tracts that coincided with the cochlear nerve identified during surgery as the vestibulocochlear nerve. Regarding identification methods for nerves, the facial nerve was identified by the presence of facial muscle action potentials elicited by direct facial nerve fascicle stimulation at 0.1–0.2 mA. With regard to the cochlear nerve, since we invented electric stimuli-elicited dorsal cochlear nucleus action potential (ESE-DNAP) monitoring [5, 9], we could identify the specific direct connection of the specific nerve fascicle with the dorsal cochlear nucleus by intraoperative electrical stimulation around 0.2–0.4 mA. Intraoperative identification of nerves was performed by the neurosurgeon who performed the surgery (H.N.). DTT visualization was performed by the first author (M.Y.), and consistency with the intraoperative findings was judged by consultation
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between a neurosurgeon (T.K.) who played no part in the surgery or preoperative DTT visualization and the first author (M.Y.).
Table 2 Prediction of nerves by diffusion tensor tractography when using variable values for the fractional anisotropy threshold and actual intraoperative findings Patient
Results Outcomes for facial nerve and hearing functions Postoperative facial nerve function according to House & Brackmann Classification was grade I in seven patients, grade II in four patients [4]. That is, all patients achieved House & Brackmann Classification grade I–III (100 %). Postoperative hearing function was graded using the Gardner-Robertson Classification [2], and was grade 1 in four patients, grade 2 in 0 patients, grade 3 in one patient, grade 4 in one patient, and grade 5 in five patients. Functional hearing (50 % speech discrimination score) was preserved in five of eight patients (62.5 %) (Table 1). Intraoperative locations of the facial and cochlear nerves in relation to VS We identified facial nerve location in all patients based on the presence of facial muscle action potentials elicited by direct stimulation of facial nerve fascicles. The facial nerve was located on the superior tumor surface in one patient, on the anterosuperior one-third of the tumor surface in seven patients, and on the anterior middle one-third of the tumor surface in three patients. We also identified cochlear nerve location in 11 patients based on the presence of ESE-DNAP elicited by direct stimulation of cochlear nerve fascicles. The cochlear nerve was located on the anteroinferior one-third of the tumor surface in seven patients, on the inferior tumor surface in three patients, and on the posterior middle one-third of the tumor surface in one patient (Table 2). Prediction by DTT and verification of prediction results Fiber tracts running from the internal auditory canal to the brainstem were visualized in ten patients. When we verified the visualized fiber tracts with the true nerves identified intraoperatively, we found agreement between the pathway area of visualized fiber tracts and the pathway area of the facial or cochlear nerves identified during surgery in nine of these ten patients. More specifically, in three of the ten patients (30 %) in whom fiber tracts were visualized, the visualized fiber tract corresponded to the pathway area of the facial nerve, and this corresponded to the pathway area of the cochlear nerve in six patients (60 %). For all 11 patients, the visualized fiber tracts corresponded to the pathway area of the facial or cochlear nerve in nine patients (81.8 %), to the pathway area of the facial nerve in three patients (27.3 %), and to the pathway area of the cochlear nerve in six patients (54.5 %) (Table 2).
Intraoperative finding
DTT outcome
Facial nerve
Cochlear nerve
1 2 3 4 5 6
AS S AS AM AS AS
AI PM AI I AI AI
AI,PI PM AI I AS,I -
7 8 9 10 11
AM AS AS AM AS
AI AI I I AI
I AS I I AS
Courses of fibers in the central portion of the cistern were classified into nine areas: S superior to the tumor; AS anterior superior one-third; AM anterior middle one-third; AI anterior inferior one-third; I inferior; PI posterior inferior one-third; PM posterior middle one-third; and PS posterior superior one-third; - not visualized
Representative cases Case 2 The patient was a 52-year-old woman who presented with hearing loss and right VS (Fig. 2a). The tumor was 20.9 mm in diameter. When FA thresholds were set at the upper limit, a fiber tract was visualized in the posterior middle one-third to the tumor (Fig. 2b–d). Surgery was performed using a lateral suboccipital approach. Electrophysiological diagnosis performed during surgery confirmed that the facial nerve ran superior to the tumor, while the cochlear nerve ran in the posterior middle one-third compared to the tumor (Fig. 2e and f). These results show that the pathway area of the visualized fiber tract corresponded with the actual pathway area of the cochlear nerve. In this patient, we intended to preserve hearing function, and therefore only performed a biopsy at that time, since resection of the tumor without injury to the cochlear nerve using a lateral suboccipital approach seemed very difficult. We subsequently performed complete resection of the tumor using an extended middle cranial fossa approach.
Case 8 The patient was a 30-year-old man who presented with hearing loss and right VS (Fig. 3a). The tumor was 28.3 mm in maximum diameter. When FA thresholds were set at the upper
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Fig. 2 Case 2. Contrast-enhanced fast imaging employing steady-state acquisition imaging shows left cerebellopontine angle vestibular schwannoma in the (a) axial view. b Axial view of diffusion tensor tractography (DTT). c Sagittal view of DTT. d Oblique view of DTT. DTT when using the upper limit of the FA threshold visualizes the fiber tract running in the posterior middle one-third to the tumor. e, f
Fig. 3 Case 8. Contrastenhanced fast imaging employing steady-state acquisition imaging showing left cerebellopontine angle vestibular schwannoma in the a axial view. b Axial view of diffusion tensor tractography (DTT). c Sagittal view of DTT. DTT when using the upper limit of the fractional anisotropy threshold visualizes the fiber tract running in the anterior superior one-third to the tumor. d Intraoperative view. Electrophysiological diagnosis performed during the surgery confirms that the facial nerve runs in the anterior superior onethird to the tumor (asterisk)
Intraoperative view. Electrophysiological diagnosis performed during the surgery confirms that the cochlear nerve passes in the posterior middle one-third to the tumor (f asterisk). Positive wave of elicited dorsal cochlear nucleus action potential (ESE-DNAP) represents the presence of the cochlear nerve (e arrowhead)
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limit, fiber tracts were visualized that ran anterior superior one-third to the tumor (Fig. 3b and c). Surgery was performed by a lateral suboccipital approach. Electrophysiological diagnosis performed during the surgery confirmed that the facial nerve ran in the anterosuperior onethird to the tumor (Fig. 3d), while the cochlear nerve passed in the anteroinferior one-third to the tumor. These results showed that the pathway area of the visualized fiber tract corresponded with the actual pathway area of the facial nerve.
Discussion In this report, we indicated for the first time that DTT allows visualization of not only the facial nerve but also the vestibulocochlear nerve in VS patients. Despite these findings, predicting whether a visualized tract represents the facial nerve, vestibulocochlear nerve, or mere noise prior to surgery is still difficult. In fact, we were uncertain whether the fiber tract visualized on DTT represented facial nerve, vestibulocochlear nerve, or mere noise in case 2, because the visualized fiber tract followed a course that the facial and vestibulocochlear nerves were considered unlikely to take [12]. The next step is therefore to develop a good method to distinguish whether a visualized tract represents facial nerve, vestibulocochlear nerve, or mere noise prior to surgery; until then, we cannot use DTT for preoperative prediction of nerve locations in relation to VS with confidence.
Comparison with results from previous reports Application of DTT to VS was first reported by Taoka et al. [14], and in a later study the preoperative visualization rate for the facial nerve was increased to 90.9 % [3]. On the other hand, visualization of the vestibulocochlear nerve was either not mentioned [1, 10] or was reported as impossible [3]. The present results are thus very different (Table 3). Three reasons can be considered for the large differences between our results and those of earlier studies. The chief reason can be surmised to be that this study set the FA threshold at the upper limit in each patient. Other possible reasons are problems with interpretation of visualized fiber tracts, and differences in the imaging equipment, imaging conditions, and software used. With regard to interpretation, as shown in this study, completely eliminating false tracts is difficult, and even if only nerve fiber tracts can be visualized, distinguishing whether a depicted fiber represents facial or vestibulocochlear nerve or noise is also problematic. As a result, even though fibers other than the facial nerve may have been visualized, previous reports have judged the visualized fiber as representing the facial nerve, thus increasing the visualization rate for the facial nerve. In particular, in cases where the cochlear and facial nerves run in parallel, errors in judgment may be made, and caution in this regard is necessary. With regard to differences in equipment and conditions, it will be necessary in the future to validate the methods described in this study by applying the same imaging conditions and software. Limitations of this study
Capacity of DTT to visualize the facial and vestibulocochlear nerves The visualized fiber tract in six patients (6/11; 54.5 %) in whom fiber tracts were visualized corresponded to the pathway area of the cochlear nerve, while in three patients (27.3 %) it corresponded to the pathway area of the facial nerve. Thus, in this study, the visualization rate was higher for the vestibulocochlear nerve than for the facial nerve. The reason for this might be that this study set the FA threshold at the upper limit for each patient. This means that nerve fiber tracts with higher FA values can be visualized at a higher rate than those with lower FA values. In addition, when we applied DTT for VS patients, the nerve fiber tract visualized by DTT as the vestibulocochlear nerve presumably included both the remnant normal vestibular nerve and the cochlear nerve, since the cochlear nerve is inseparable from the vestibular nerve at the brainstem and cerebellopontine segments. As a result, FA values of the nerve fiber tract visualized as the vestibulocochlear nerve were higher than those of the facial nerve, leading to a higher rate of vestibulocochlear nerve visualization by DTT.
In this study, the upper limit of the FA threshold was set for each patient. As a result, the facial or vestibulocochlear nerve was visualized in nine of 11 VS patients. However, increasing the FA threshold and setting the upper limit decreased not only the noise but also the visualization of actual nerve fiber tracts. We cannot rule out the possibility that this led to a decrease in the predictive value for the facial nerve compared with earlier reports. Another problem is the current visualization capacity of DTT. We still have no good method for distinguishing in advance whether a visualized fiber represents facial nerve, vestibulocochlear nerve, or simply noise, which would decrease the reliability of DTT for preoperative prediction of nerve location. The present results revealed that the fibers visualized when the FA threshold is at the upper limit show a strong tendency to coincide with the course of the vestibulocochlear nerve. The results of this study may contribute to the development of methods for distinguishing the vestibulocochlear nerve from the facial nerve and noise, and further studies of a greater number of cases are warranted. Imaging conditions for DTT also need to be investigated further.
Visualization rate of cochlear nerve (%)
Not mentioned
Not verified
0.0
Not mentioned
66.6
Visualization rate of facial nerve (%)
62.5
Not verified
90.9
100
25.5
Seed ROI
Placement at the fundus of the internal auditory meatus on the sagittal cross section Placement at the intracanalicular compartment for the facial/ vestibular complex Placement to the internal auditory meatus Placement at around the circumference of the tumor in a midcisternal portion on the sagittal cross section Placement at the porus of the internal auditory meatus on a plane perpendicular to the facial and vestibulocochlear nerves
Conclusions In this study, DTT was proved to be able to visualize not only the facial nerve but also the vestibulocochlear nerve, which has been considered difficult to achieve with conventional visualization methods. Despite our findings, good methods for distinguishing whether a visualized nerve tract represents facial nerve, vestibulocochlear nerve, or noise remain unavailable. Close attention should therefore be paid to the interpretation of visualized fibers. Acknowledgments This work was supported in part by Grant-in-Aid for Challenging Exploratory Research 25670618. We wish to thank Minoru Tanaka for suggesting this investigation. Conflict of interest None.
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Upper limit for each patient
0.15
0.1
0.2
0.1
FA threshold
2. 3.
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3D slicer
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Software
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Vestibular schwannoma Cerebellopontine angle tumor Gergnov et al. [3], 2010 Roundy et al. [10], 2012
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Vestibular schwannoma Chen et al. [1] 2007
27.0 (mean)
29 (mean) Vestibular schwannoma Taoka et al. [14], 2006
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Tumor diameter (mm) Test subject
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Table 3
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Comments The authors describe a novel modification of a DTI/DTT technique to identify the cochlear nerve by increasing the fraction anisotropy (FA) threshold. While this technique decreases the ability to identify facial nerves, it has a merit in identifying the cochlear nerve, which would be of importance if a hearing-preservation surgery is planned. The identification of vestibular nerves and potential misinterpretation between the vestibular nerve and cochlear nerve is a major concern with this method. Future modification of this technique will hopefully enable us to obtain accurate identification of both facial and cochlear nerves by adjusting the FA threshold in the same setting and identifying different cranial nerve trajectory. Amir Dehdashti NY, USA
