DSC perfusion MR imaging in brain tumors requires a trade-off between spatial and temporal resolution, resulting in less spatial coverage to meet the temporal resolution requirements for accurate relative CBV estimation. DSC-MR imaging could potentially benefit from the advantages associated with simultaneous multi-slice imaging, including increased spatiotemporal resolution. In the current article, we demonstrate how simultaneous multi-slice EPI can be used to improve DSC-MR imaging spatiotemporal resolution in patients with glioblastoma

Chakhoyan, A

Cloughesy, TF

Ellingson, BM

Leu, K

Pope, WB

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UCLAUCLA Previously Published WorksTitleImproved Spatiotemporal Resolution of Dynamic Susceptibility Contrast Perfusion MRI in Brain Tumors Using Simultaneous Multi-Slice Echo-Planar ImagingPermalinkhttps://escholarship.org/uc/item/3sx3j0zkJournalAmerican Journal of Neuroradiology, 39(1)ISSN0195-6108AuthorsChakhoyan, ALeu, KPope, WBet al.Publication Date2018DOI10.3174/ajnr.a5433 Peer reviewedeScholarship.org Powered by the California Digital LibraryUniversity of CaliforniaBRIEF/TECHNICAL REPORTADULT BRAINImproved Spatiotemporal Resolution of DynamicSusceptibility Contrast Perfusion MRI in Brain Tumors UsingSimultaneous Multi-Slice Echo-Planar ImagingX A. Chakhoyan, X K. Leu, X W.B. Pope, X T.F. Cloughesy, and X B.M. EllingsonABSTRACTSUMMARY: DSC perfusion MR imaging in brain tumors requires a trade-off between spatial and temporal resolution, resulting in lessspatial coverage to meet the temporal resolution requirements for accurate relative CBV estimation. DSC-MR imaging could potentiallybenefit from the advantages associated with simultaneous multi-slice imaging, including increased spatiotemporal resolution. In thecurrent article, we demonstrate how simultaneous multi-slice EPI can be used to improve DSC-MR imaging spatiotemporal resolution inpatients with glioblastoma.ABBREVIATIONS: rCBV  relative CBV; SMS  simultaneous multi-sliceDSC perfusion MR imaging estimates of relative CBV (rCBV)have been shown to differentiate histologic tumor grade,1,2predict survival, and be useful for therapeutic monitoring in braintumors3; however, DSC requires compromises in image resolu-tion, slice coverage, and temporal resolution. The TR must beshort enough to capture the rapid passage of the contrast bolusthrough the blood vasculature, but at the same time, there must beenough spatial coverage to encapsulate the entire tumor or brain.Simultaneous multi-slice (SMS) EPI4 has drawn widespread at-tention due to the advent of highly accelerated images5 throughthe application of composite radiofrequency pulses to simultane-ously excite multiple slice planes.6 The SMS technique excitesmultiple slices physically separated across the z-axis simultane-ously so that each SMS “slab” has slices acquired interleavedwithin that section. SMS has been shown to not have appreciableloss in SNR compared with traditional methods,4 and studies haveshown that SMS is effective in reducing the acquisition time withhigher spatiotemporal resolution.5,7,8 In the current article, wedemonstrate the clinical utility of using SMS-EPI to increase thespatiotemporal resolution of DSC-MR imaging in patients withglioblastoma.MATERIALS AND METHODSPatientsThirteen patients with pathologically confirmed primary glioblas-toma with recurrence based on either MR imaging, clinical dete-rioration, and/or histology were enrolled in this prospectivestudy, which was approved by our local ethics institutional reviewboard (University of California, Los Angeles). All patients under-went DSC-MR imaging with conventional single-shot EPI fol-lowed by SMS-EPI, 1–2 months later.DSC-MR Imaging AcquisitionA preload bolus of 0.025 mmol/kg of Gd-DTPA (Magnevist;Bayer HealthCare Pharmaceuticals, Wayne, New Jersey) was ad-ministered to reduce leakage effects followed by 0.075 mmol/kg ofGd-DTPA at a rate of 5 mL/s. Two minutes of data were acquired,including a 30-second prebolus baseline and 90 seconds of dataduring and following contrast injection.Conventional DSC-MR imaging was then acquired using asingle-shot gradient-echo EPI at 3T (Prisma; Siemens, Erlangen,Germany) with TE  35 ms, TR  1.25–1.9 seconds, flip angle 60°, FOV  24  24 cm, matrix size  128  128, generalizedReceived April 30, 2017; accepted after revision August 24.From the UCLA Brain Tumor Imaging Laboratory (A.C., K.L., B.M.E.), Center forComputer Vision and Imaging Biomarkers, University of California, Los Angeles, LosAngeles, California; Departments of Radiological Sciences (A.C., K.L., W.B.P., B.M.E.),Biomedical Physics (B.M.E.), Psychiatry and Biobehavioral Sciences (B.M.E.), UCLABrain Research Institute (T.F.C., B.M.E.), and Neurology (T.F.C.), David Geffen Schoolof Medicine, University of California, Los Angeles, Los Angeles, California; and De-partment of Bioengineering (K.L., B.M.E.), Henry Samueli School of Engineering andApplied Science, and UCLA Neuro-Oncology Program (T.F.C., B.M.E.), University ofCalifornia, Los Angeles, Los Angeles, California.This work was supported by the American Cancer Society Research Scholar GrantRSG-15-003-01-CCE (B.M.E.); the National Institutes of Health/National Cancer In-stitute R21CA167354 (B.M.E.); an American Brain Tumor Association Research Col-laboration Grant supported by Humor to Fight the Tumor, ARC1700002 (B.M.E.);a National Brain Tumor Society research grant (B.M.E.); a National Institutes ofHealth/National Institute of General Medical Sciences training grant, GM08042(K.L.); and the University of California, Los Angeles Medical Scientist TrainingProgram (K.L.).Please address correspondence to Benjamin M. Ellingson, PhD, Departments ofRadiological Sciences and Psychiatry, David Geffen School of Medicine, Universityof California, Los Angeles, 924 Westwood Blvd, Suite 615, Los Angeles, CA 90024;e-mail: bellingson@mednet.ucla.edu; @ben_ellingsonIndicates open access to non-subscribers at www.ajnr.orghttp://dx.doi.org/10.3174/ajnr.A5433AJNR Am J Neuroradiol ●:● ● 2018 www.ajnr.org 1 Published October 26, 2017 as 10.3174/ajnr.A5433 Copyright 2017 by American Society of Neuroradiology.autocalibrating partially parallel acquisition  2, slice thickness 5 mm with no interslice gap, and 15- to 20-slice coverage. Thevoxel size was 1.875  1.875  5 mm, and the temporal resolutionwas 1.25–1.90 seconds.Accelerated DSC-MR imaging was obtained with single-shotSMS-EPI with TE  35ms, TR  750 ms, flip angle  60°, FOV 21.6  24 cm, matrix size  180  200, slice thickness  4 mmwith no interslice gap, controlled aliasing in parallel imaging re-sults in higher acceleration factor  2, and an SMS accelerationfactor of 4 for a total of 30 slices through the whole brain. Voxelsizes were 1.2  1.2  4 mm with temporal resolution of 0.75seconds.Postprocessing of DSC-MR ImagingRelative cerebral blood volume maps were generated with customscripts including correction for bidirectional contrast agent ex-change between the vascular and extravascular space.9 All rCBVvalues were normalized to contralateral normal-appearing whitematter.ROI and Statistical AnalysesContrast-enhancing tumor ROIs were defined in 3D using cus-tom scripts from Analysis of Functional Neuro Images (AFNI;http://afni.nimh.nih.gov/afni), excluding hemorrhage, largevessels, and central necrosis, followed by manual editing toexclude nonlesional voxels.9 Additionally, 2-cm-diameter sphericROIs were placed on contralateral normal-appearing whitematter for normalization of rCBV measurements. The percent-age difference in the mean rCBV ratio, maximum tumor rCBVdifference, and voxelwise correlations between single-shot EPIand SMS-EPI were estimated from the resulting data for all 13patients. GraphPad Prism software, Version 6.0h (GraphPadSoftware, San Diego, California) was used for all statisticalanalyses.RESULTSBoth raw DSC and calculated rCBV maps were of comparablequality; however, rCBV maps calculated with SMS-EPI were ob-tained for the entire brain and at slightly higher spatial resolutioncompared with rCBV maps obtained with conventional single-shot EPI (Fig 1A, -B). The mean tumor rCBV difference betweenthese 2 techniques was 4.7%  0.6% (Fig 1C), and the maximumtumor rCBV difference was 10.8%  1.2% (Fig 1D). Voxelwisecorrelations in rCBV between the 2 techniques showed a signifi-cant association in all patients examined (Fig 1E), with rCBV ra-tios in the tumor with respect to normal-appearing white matterslightly higher when estimated using SMS-EPI.FIG 1. Postcontrast T1-weighted images, T2-weighted FLAIR images, and raw T2*-weighted DSC MR images with corresponding signal-timecurves across time from tumor regions accompanied by resulting relative cerebral blood volume maps for conventional single-shot EPI (A) andsimultaneous multi-slice EPI (B) (left to right). Percentage difference in mean tumor rCBV ratio (tumor to normal-appearing white matter) (C) andpercentage difference in the maximum tumor rCBV ratio (tumor to normal-appearing white matter) (D) in 13 patients with recurrent glioblas-toma. E, Voxelwise correlation of rCBV ratio between conventional single-shot EPI and SMS-EPI.2 Chakhoyan ● 2018 www.ajnr.orgCONCLUSIONSSMS-EPI can increase the spatiotemporal resolution in DSC-MRimaging, resulting in larger brain coverage (12 versus 10 cm),higher in-plane spatial resolution (1.2  1.2  4 mm versus1.875  1.875  5 mm), and faster temporal resolution (0.75versus 1.25–1.90 seconds), with comparable results in quantifica-tion of tumor vascularity and clinical feasibility. While the poten-tial impact on slice-to-slice perfusion quantitation is not currentlyknown and results suggest that there may be little effect, a largerstudy is warranted. Together, these data demonstrate the poten-tial clinical value of using SMS-EPI to estimate rCBV in patientswith brain tumors with a high degree of reproducibility in termsof vascular biology quantification compared with historical test-retest studies.10Disclosures: Whitney B. Pope—RELATED: Consulting Fee or Honorarium: Bracco;UNRELATED: Grants/Grants Pending: Guerbet.* Benjamin M. Ellingson—RELATED:Grant: Siemens; UNRELATED: Board Membership: MedQIA, Medicenna, Roche, AgiosPharmaceuticals, Bristol-Myers Squib; Consultancy: MedQIA, Medicenna, Roche, AgiosPharmaceuticals, Bristol-Myers Squib. *Money paid to the institution.REFERENCES1. Aronen HJ, Gazit IE, Louis DN, et al. Cerebral blood volume maps ofgliomas: comparison with tumor grade and histologic findings. Ra-diology 1994;191:41–51 CrossRef Medline2. Cha S, Knopp EA, Johnson G, et al. Intracranial mass lesions: dy-namic contrast-enhanced susceptibility-weighted echo-planar per-fusion MR imaging. Radiology 2002;223:11–29 CrossRef Medline3. Law M, Yang S, Wang H, et al. Glioma grading: sensitivity, specific-ity, and predictive values of perfusion MR imaging and proton MRspectroscopic imaging compared with conventional MR imaging.AJNR Am J Neuroradiol 2003;24:1989 –98 Medline4. Barth M, Breuer F, Koopmans PJ, et al. Simultaneous multislice(SMS) imaging techniques. Magn Reson Med 2016;75:63–81 CrossRefMedline5. Feinberg DA, Moeller S, Smith SM, et al. Multiplexed echo planarimaging for sub-second whole brain FMRI and fast diffusion imag-ing. PLoS One 2010;5:e15710 CrossRef Medline6. Maudsley AA. Multiple-line-scanning spin density imaging. J MagnReson 1980;41:112–267. Chen L, T Vu A, Xu J, et al. Evaluation of highly accelerated simul-taneous multi-slice EPI for fMRI. Neuroimage 2015;104:452–59CrossRef Medline8. Feinberg DA, Setsompop K. Ultra-fast MRI of the human brain withsimultaneous multi-slice imaging. J Magn Reson 2013;229:90 –100CrossRef Medline9. Ellingson BM, Cloughesy TF, Lai A, et al. Quantitative volumetricanalysis of conventional MRI response in recurrent glioblastomatreated with bevacizumab. Neuro Oncol 2011;13:401– 09 CrossRefMedline10. Henry ME, Kaufman MJ, Lange N, et al. Test-retest reliability ofDSC MRI CBV mapping in healthy volunteers. 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Improved Spatiotemporal Resolution of Dynamic Susceptibility Contrast Perfusion MRI in Brain Tumors Using Simultaneous Multi-Slice Echo-Planar Imaging

Improved Spatiotemporal Resolution of Dynamic Susceptibility Contrast Perfusion MRI in Brain Tumors Using Simultaneous Multi-Slice Echo-Planar Imaging.

Improved Spatiotemporal Resolution of Dynamic Susceptibility Contrast Perfusion MRI in Brain Tumors Using Simultaneous Multi-Slice Echo-Planar Imaging.

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