Slip interface imaging: a novel MR-elastography based imaging method for assessing the surgical plane of cleavage in meningiomas
Ziying Yin1, Kevin J. Glaser1, Armando Manduca2, Jamie J. Van Gompel3, Arvin Arani1, Joshua D. Hughes3, Anthony Romano4, Richard L. Ehman1, and John Huston III1

1Radiology, Mayo Clinic, Rochester, MN, United States, 2Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, United States, 3Neurosurgery, Mayo Clinic, Rochester, MN, United States, 4Naval Research Laboratory, Washington, WA, United States

Synopsis

The preoperative assessment of the surgical cleavage plane at the tumor-brain interface in meningiomas is important for surgical planning. A recently developed slip interface imaging (SII) technique is uniquely capable of directly assessing the degree of tumor adherence at the tumor-brain interface. In this study, SII was applied to assess the surgical cleavage plane between the tumor and the underlying brain in meningiomas. The correlation between the SII results and the surgical plane of cleavage was statistically significant (p=0.0014). The presence of a complete slip interface suggests the tumor can be removed using a dissection plane outside the pia mater.

PURPOSE

The preoperative assessment of the surgical cleavage plane at the tumor-brain interface in meningiomas is important for surgical planning and accurate assessment of post-surgical prognosis. Meningiomas that are adherent are much more difficult to resect resulting in extended surgical procedures, increased risk of complications and incomplete tumor removal, which could lead to tumor recurrence1. Previous studies have described the usefulness of MRI, CT, and angiography in predicting the cleavage plane of meningiomas2,3. However, these studies do not provide a direct measure of the degree of tumor cleavage, i.e., the degree of tumor adherence at the tumor-brain interface. A recently developed slip interface imaging (SII) technique is uniquely capable of directly assessing the tumor-brain interface. This technique has been successfully applied to assess the tumor-brainstem adhesion in vestibular schwannomas4. The goal of this study was to determine the extent to which SII can be used to assess the surgical cleavage plane between the tumor and the underlying brain in meningiomas.

METHODS

With institutional review board approval and written informed consent, 20 patients (5M and 15F, 61±11 years) with pathologically proven meningiomas underwent the preoperative MRI and SII assessments on 3T MR scanners. The SII technique is based on MR elastography (MRE)4. Low amplitude mechanical vibrations at 60 Hz were introduced into the head with a pillow-like MRE driver. The resulting shear waves were imaged by a single-shot, flow-compensated, SE-EPI MRE pulse sequence with the same scanning parameters as reference (4). The MR phase data were processed by shear line analysis to generate shear line images and quantitative octahedral shear strain (OSS) maps as described in reference (4). According to the criteria in Table 1, SII results were classified into three categories: complete slip interface (SI), partial SI, and no SI, and then correlated with three types of surgical cleavage planes (extrapial, mixed, and subpial) encountered at surgery. The correlation was assessed by using the Chi-square test (significance level <0.05). The Cohen κ coefficient was used to study the agreement between the SII prediction and surgical findings.

RESULTS

The slip interface between the tumor and the brain was represented as a hypo-intensity contour on shear line images and high OSS values along the interface. Figure 1 shows a representative case illustrating a tumor with complete SI, where the tumor was completely removed via an extrapial surgical plane. A tumor with the absence of a well-delineated slip interface in Figure 2 was classified as no SI, and a subpial plane was found at surgery. As shown in Table 2, SII agreed with the intraoperative assessment in 15 (75%) of 20 cases (moderate agreement: κ=0.52). Twelve (87%) of the 14 tumors with complete SI had an extrapial plane, but the other two had mixed plane findings. When a tumor was classified as partial or no SI, the surgical plane was non-extrapial. Overall, the correlation between the SII results and the surgical plane of cleavage was statistically significant (p=0.0014).

DISCUSSION

In all of the 12 cases with a surgical extrapial plane of cleavage, SII demonstrated a well-delineated complete SI on both shear line image and OSS maps. The results clearly show that a complete SI may be a predictor of an extrapial plane. If a safe (i.e. extrapial) surgical plane of cleavage exists, the low-amplitude (~microns) mechanical vibration of SII can lead to a large differential motion between the tumor and the adjacent brain surface on both sides of the interface due to the loose connection. This relative motion can create a large phase shift across the interface, leading to a signal loss at the interface due to intravoxel phase dispersion5. The large shear deformation caused by a slip boundary can also be captured at the same time by measuring OSS, which reflects the maximum shear strain across all possible planes. However, in patients with a non-extrapial (mixed or subpial) surgical plane, 5 of the 8 cases were discordant. Our findings showed that the discrepancies mostly happened in the tumors with prominent adjacent edema, calcified rim or portions, or internal cysts. The existence of these multiple tissue planes inside or outside the tumor likely complicates shear motions at tumor boundaries, which could interfere with the SII predictions. Future studies will focus on understanding and improving the accuracy of SII prediction of surgical planes with a larger patient cohort.

CONCLUSION

SII can provide a method for preoperative prediction of the surgical plane of tumor cleavage in meningiomas. The presence of a complete SI suggests that the tumor can be removed using a dissection plane outside the pia mater.

Acknowledgements

This work was supported in part by grants from the National Institute of Health RO1 EB001981 and an Office of Naval Research Contract N00173-15-P-0618.

References

1. Violaris K, Katsarides V, Sakellariou P. The Recurrence Rate in Meningiomas: Analysis of Tumor Location, Histological Grading, and Extent of Resection. Open Journal of Modern Neurosurgery. 2012; 2(1): 6-10.

2. lvernia 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(3):422–430.

3. Celikoglu E, Suslu HT, Hazneci J, Bozbuga M. The relation between surgical cleavage and preoperative neuroradiological findings in intracranial meningiomas. European Journal of Radiology. 2011; 80(2): 108-115.

4. Yin Z, Glaser KJ, Manduca A, Van Gompel JJ, Link JM, Hughes JD, Romano A, Ehman RL, Huston J. Slip Interface Imaging Predicts Tumor-Brain Adhesion in Vestibular Schwannomas. Radiology. 2015; 277: 507-517

5. Mariappan YK, Glaser KJ, Manduca A, Ehman RL. Cyclic motion encoding for enhanced MR visualization of slip interfaces. J Magn Reson Imaging 2009;30(4):855–863.

Figures

Figure 1. (a) T2-weighted FLAIR image of a falcine meningioma. (b) Shear line image. (c) OSS map. The slip interface can be observed as a hypo-intense shear line with large OSS values around more than 2/3 of the tumor-brain interface (complete SI). Surgical findings demonstrated an extrapial surgical plane.

Figure 2. (a) T2-weighted FLAIR image of a left cerebellopontine angle meningioma. (b) Shear line image. (c) OSS map. No shear line hypo-intensity or large OSS values exist along the tumor boundary indicating no slip interface, which correlated with the surgical findings of extreme tumor adherence to cerebellum and brainstem.

Table 1. Classification of SII predictions and surgical planes of cleavage

Table2. Agreement between SII prediction and surgical findings



Proc. Intl. Soc. Mag. Reson. Med. 24 (2016)
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