Slip interface imaging based on MR-elastography preoperatively predicts meningioma-brain adhesion

Ziying Yin, Joshua D Hughes, Joshua D Trzasko, Kevin J Glaser, Armando Manduca, Jamie Van Gompel, Michael J Link, Anthony Romano, Richard L Ehman, John Huston 3rd, Ziying Yin, Joshua D Hughes, Joshua D Trzasko, Kevin J Glaser, Armando Manduca, Jamie Van Gompel, Michael J Link, Anthony Romano, Richard L Ehman, John Huston 3rd

Abstract

Purpose: To investigate the ability of slip interface imaging (SII), a recently developed magnetic resonance elastography (MRE)-based technique, to predict the degree of meningioma-brain adhesion, using findings at surgery as the reference standard.

Materials and methods: With Institutional Review Board approval and written informed consent, 25 patients with meningiomas >2.5 cm in maximal diameter underwent preoperative SII assessment. Intracranial shear motions were introduced using a soft, pillow-like head driver and the resulting displacement field was acquired with an MRE pulse sequence on 3T MR scanners. The displacement data were analyzed to determine tumor-brain adhesion by assessing intensities on shear line images and raw as well as normalized octahedral shear strain (OSS) values along the interface. The SII findings of shear line images, OSS, and normalized OSS were independently and blindly correlated with surgical findings of tumor adhesion by using the Cohen's κ coefficient and chi-squared test.

Results: Neurosurgeons categorized the surgical plane as extrapial (no adhesion) in 15 patients, mixed in four, and subpial (adhesion) in six. Both shear line images and OSS agreed with the surgical findings in 18 (72%) cases (fair agreement, κ = 0.37, 95% confidence interval [CI]: 0.05-0.69), while normalized OSS was concordant with the surgical findings in 23 (92%) cases (good agreement, κ = 0.86, 95% CI: 0.67-1). The correlation between SII predictions (shear line images, OSS, and normalized OSS) and the surgical findings were statistically significant (chi-squared test, P = 0.02, P = 0.02, and P < 0.0001, respectively).

Conclusion: SII preoperatively evaluates the degree of meningioma-brain adhesion noninvasively, allowing for improved prediction of surgical risk and tumor resectability.

Level of evidence: 1 Technical Efficacy: Stage 1 J. Magn. Reson. Imaging 2017;46:1007-1016.

Keywords: magnetic resonance elastography; meningioma; octahedral shear strain; slip interface imaging; surgical plane; tumor-brain adhesion.

© 2017 The Authors Journal of Magnetic Resonance Imaging published by Wiley Periodicals, Inc. on behalf of International Society for Magnetic Resonance in Medicine.

Figures

Figure 1
Figure 1
Bar graphs showing the correlation between slip interface imaging and surgical findings. Left: shear line imaging (P = 0.02, chi‐squared test); Middle: OSS (P = 0.02, chi‐squared test); Right: normalized OSS (P < 0.0001, chi‐squared test).
Figure 2
Figure 2
Concordant case with a complete slip interface at imaging and no adhesion at surgery (case 14, 63‐year‐old male). a: T1‐weighted image with contrast enhancement shows a large left medial sphenoid wing meningioma. The tumor–brain interface is clearly defined with the (b) shear line image, (c) OSS map, and (d) normalized OSS map (arrows), indicating the presence of the slip interface and no adhesion. Surgical findings demonstrated that the dissection plane was nearly completely extrapial with no meningioma–brain adhesion encountered.
Figure 3
Figure 3
Concordant case with a partial slip interface at imaging and partial adhesion at surgery (case 17, 49‐year‐old female). a: Sagittal T1‐weighted image with contrast enhancement shows a petroclival meningioma. The tumor–brain interface is partially defined in the (b) shear line image, (c) OSS map, and (d) normalized OSS map with arrows indicating the presence of a slip interface and arrowheads indicating the absence of a slip interface, suggesting the tumor was partially adherent to the brainstem. At surgery the dissection plane was also classified as mixed adhesion, corresponding to the SII findings.
Figure 4
Figure 4
Concordant case with no slip interface on imaging and adhesion at surgery (case 22, 55‐year‐old, female). a: T1‐weighted image with contrast enhancement shows a left cerebellopontine angle meningioma. No apparent slip interface is identified with the (b) shear line image, (c) OSS map, or (d) normalized OSS map (arrows), suggesting tumor–brainstem and tumor–cerebellum adhesion. Surgical findings demonstrated a subpial plane with meningioma–brain adhesion and a very difficult resection.
Figure 5
Figure 5
Discordant case of a tumor that was predicted correctly by normalized OSS but not by shear line image or OSS (case 24, 46‐year‐old, female). a: T1‐weighted image with contrast enhancement shows a right lateral sphenoid wing meningioma. b: T2‐weighted image reveals peritumoral edema (arrowhead). (c) Shear line image with low signal and (d) high values on the OSS map predicted complete slip interface with no adhesion (arrows). Normalized OSS map (e) suggested no slip interface with adhesion, as no apparent tumor outline was identified. Intraoperatively, the meningioma was very adherent, with the pia largely invaded completely around the tumor.
Figure 6
Figure 6
Discordant case by normalized OSS but correctly predicted with shear line image and OSS (case 15, 76‐year‐old, male). a: T2‐weighted image shows a right frontal convexity meningioma. b: Shear line image with low surrounding signal and (c) high values on the OSS map predicted a complete slip interface with no adhesion (arrows). However, half of the contour was not seen in the normalized OSS map (d), suggesting partial adhesion. Surgical findings demonstrated an extrapial plane with no meningioma–brain adhesion.
Figure 7
Figure 7
Discordant case between SII and surgical findings (case 19, 80‐year‐old, female). a: T1‐weighted image with contrast enhancement shows a right parasagittal meningioma with a lateral portion that was noncontrast‐enhancing (arrowhead). The rim of the tumor is clearly defined with (b) shear line image, (c) OSS map, and (d) normalized OSS map (arrows), suggesting no adhesion. However, surgical findings demonstrated that the tumor was adherent to the anterior and posterior cortex.

References

    1. Mirimanoff RO, Dosoretz DE, Linggood RM, Ojemann RG, Martuza RL. Meningioma: analysis of recurrence and progression following neurosurgical resection. J Neurosurg 1985;62:18–24.
    1. Couldwell WT, Fukushima T, Giannotta SL, Weiss, MH . Petroclival meningiomas: surgical experience in 109 cases. J Neurosurg 1996;84:20–28.
    1. Sekhar LN, Swamy NKS, Jaiswal V, et al. Surgical excision of meningiomas involving the clivus: preoperative and intraoperative features as predictors of postoperative functional deterioration. J Neurosurg 1994;81:860–868.
    1. van Alkemade H, de Leau M, Dieleman EM, et al. Impaired survival and long‐term neurological problems in benign meningioma. Neuro Oncol 2012;14:658–666.
    1. Ýldan F, Tuna M, Göcer AÝ, et al. Correlation of the relationships of brain‐tumor interfaces, magnetic resonance imaging, and angiographic findings to predict cleavage of meningiomas. J Neurosurg 1999;91:384–390.
    1. Alvernia JE, Sindou MP. Preoperative neuroimaging findings as a predictor of the surgical plane of cleavage: prospective study of 100 consecutive cases of intracranial meningioma. J Neurosurg 2004;100:422–430.
    1. Celikoglu E, Suslu HT, Hazneci J, Bozbuga M. The relation between surgical cleavage and preoperative neuroradiological findings in intracranial meningiomas. Eur J Radiol 2011;80:e109–115.
    1. Yin Z, Glaser KJ, Manduca A, et al. Slip interface imaging predicts tumor‐brain adhesion in vestibular schwannomas. Radiology 2015;277:507–517.
    1. Mariappan YK, Glaser KJ, Manduca A, Ehman RL. Cyclic motion encoding for enhanced MR visualization of slip interfaces. J Magn Reson Imaging 2009;30:855–863.
    1. Murphy MC, Huston J 3rd, Glaser KJ, et al. Preoperative assessment of meningioma stiffness using magnetic resonance elastography. J Neurosurg 2013;118:643–648.
    1. McGarry MD, Van Houten EE, Perrinez PR, Pattison AJ, Weaver JB, Paulsen KD. An octahedral shear strain‐based measure of SNR for 3D MR elastography. Phys Med Biol 2011;56:N153–164.
    1. Glaser KJ, Felmlee JP, Manduca A, Kannan Mariappan Y, Ehman RL. Stiffness‐weighted magnetic resonance imaging. Magn Reson Med 2006;55:59–67.
    1. Xu ZS, Lee RJ, Chu SS, et al. Evidence of changes in brain tissue stiffness after ischemic stroke derived from ultrasound‐based elastography. J Ultrasound Med 2013;32:485–494.
    1. Thitaikumar A, Ophir J. Effect of lesion boundary conditions on axial strain elastograms: a parametric study. Ultrasound Med Biol 2007;33:1463–1467.
    1. Papazoglou S, Hamhaber U, Braun J, Sack I. Horizontal shear wave scattering from a nonwelded interface observed by magnetic resonance elastography. Phys Med Biol 2007;52:675–684.
    1. Yamada S, Taoka T, Nakagawa I, et al. A magnetic resonance imaging technique to evaluate tumor‐brain adhesion in meningioma: brain‐surface motion imaging. World Neurosurg 2015;83:102–107.
    1. Arun T, Thomas AK, Brian SG, Jonathan O. Visualization of bonding at an inclusion boundary using axial–shear strain elastography: a feasibility study. Phys Med Biol 2007;52:2615.
    1. Chakraborty A, Bamber JC, Dorward NL. Slip elastography: A novel method for visualising and characterizing adherence between two surfaces in contact. Ultrasonics 2012;52:364–376.

Source: PubMed

Sponsoren und Mitarbeiter

Krankheiten

Drogeninterventionen

3
Abonnieren