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 recurrence
1. Previous studies
have described the usefulness of MRI, CT, and angiography in predicting the
cleavage plane of meningiomas
2,3. 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 schwannomas
4. 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 dispersion
5. 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
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