Reduced field of view echo-planar imaging diffusion tensor MRI for pediatric spinal tumors

Restricted access

OBJECTIVE

Spine MRI is a diagnostic modality for evaluating pediatric CNS tumors. Applying diffusion-weighted MRI (DWI) or diffusion tensor imaging (DTI) to the spine poses challenges due to intrinsic spinal anatomy that exacerbates various image-related artifacts, such as signal dropouts or pileups, geometrical distortions, and incomplete fat suppression. The zonal oblique multislice (ZOOM)–echo-planar imaging (EPI) technique reduces geometric distortion and image blurring by reducing the field of view (FOV) without signal aliasing into the FOV. The authors hypothesized that the ZOOM-EPI method for spine DTI in concert with conventional spinal MRI is an efficient method for augmenting the evaluation of pediatric spinal tumors.

METHODS

Thirty-eight consecutive patients (mean age 8 years) who underwent ZOOM-EPI spine DTI for CNS tumor workup were retrospectively identified. Patients underwent conventional spine MRI and ZOOM-EPI DTI spine MRI. Two blinded radiologists independently reviewed two sets of randomized images: conventional spine MRI without ZOOM-EPI DTI, and conventional spine MRI with ZOOM-EPI DTI. For both image sets, the reviewers scored the findings based on lesion conspicuity and diagnostic confidence using a 5-point Likert scale. The reviewers also recorded presence of tumors. Quantitative apparent diffusion coefficient (ADC) measurements of various spinal tumors were extracted. Tractography was performed in a subset of patients undergoing presurgical evaluation.

RESULTS

Sixteen patients demonstrated spinal tumor lesions. The readers were in moderate agreement (kappa = 0.61, 95% CI 0.30–0.91). The mean scores for conventional MRI and combined conventional MRI and DTI were as follows, respectively: 3.0 and 4.0 for lesion conspicuity (p = 0.0039), and 2.8 and 3.9 for diagnostic confidence (p < 0.001). ZOOM-EPI DTI identified new lesions in 3 patients. In 3 patients, tractography used for neurosurgical planning showed characteristic fiber tract projections. The mean weighted ADCs of low- and high-grade tumors were 1201 × 10−6 and 865 × 10−6 mm2/sec (p = 0.002), respectively; the mean minimum weighted ADCs were 823 × 10−6 and 474 × 10−6 mm2/sec (p = 0.0003), respectively.

CONCLUSIONS

Diffusion MRI with ZOOM-EPI can improve the detection of spinal lesions while providing quantitative diffusion information that helps distinguish low- from high-grade tumors. By adding a 2-minute DTI scan, quantitative diffusion information and tract profiles can reliably be obtained and serve as a useful adjunct to presurgical planning for pediatric spinal tumors.

ABBREVIATIONS ADC = apparent diffusion coefficient; DTI = diffusion tensor imaging; DWI = diffusion-weighted imaging; EPI = echo-planar imaging; FA = fractional anisotropy; FOV = field of view; ROI = region of interest; ZOOM = zonal oblique multislice.

Article Information

Correspondence Kristen W. Yeom: Lucile Packard Children’s Hospital, Stanford University School of Medicine, Palo Alto, CA. kyeom@stanford.edu.

INCLUDE WHEN CITING Published online July 5, 2019; DOI: 10.3171/2019.4.SPINE19178.

Disclosures Dr. Aksoy: direct stock ownership in HobbitView, Inc., and consultant for Ischemaview, Inc.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    The ZOOM-EPI technique,19,33 which uses a tilted refocusing pulse followed by a 90° slice selective pulse, and a 180° pulse applied obliquely. The resulting parallelogram (shaded dark green area) of excited tissue corresponds to the desired rectangular volume. Figure is available in color online only.

  • View in gallery

    Reduction of distortion as one moves from a full FOV EPI (A) to a rectangular FOV with ZOOM-EPI (B). For the parameters used in this work, this “distortion meter” accompanying the trajectories is drawn to scale. kx and ky refer to the x (horizontal) and y (vertical) axes of k-space, an abstract concept for the image space storing raw data obtained by MRI before mathematical processing. Figure is available in color online only.

  • View in gallery

    Thoracic and cervical b = 0 images demonstrating positive distortion (+), negative distortion (-), and the average of both directions of distortion (Avg). A and C: b = 0 images where no distortion correction has been applied. B and D: The same images after performing distortion correction with the displacement field calculated from the positive (+) and negative (-) images.

  • View in gallery

    Flowchart illustrating the image acquisition and evaluation process.

  • View in gallery

    Average reviewer grades as measured by Likert scale scores from MR images obtained in 38 patients with or without the addition of performed ZOOM-EPI DTI of the spine, read by the first reviewer (A) and the second reviewer (B). Figure is available in color online only.

  • View in gallery

    Images obtained in a 6-year-old girl with a brainstem pilocytic astrocytoma. Sagittal contrast-enhanced T1-weighted image (A), sagittal diffusion-weighted image (B), sagittal ADC (C), sagittal FA (D), and sagittal colored FA map (E). Note the position of the fourth ventricle relative to mass. Figure is available in color online only.

  • View in gallery

    Images obtained in a 5-year-old boy with infiltrating grade II astrocytoma. Sagittal b = 0 (A), iso-diffusion-weighted image (B), color FA (C), and tractography (D and E). Note the tract profiles traversing within this infiltrating spinal cord tumor. Figure is available in color online only.

References

  • 1

    Abul-Kasim KThurnher MMMcKeever PSundgren PC: Intradural spinal tumors: current classification and MRI features. Neuroradiology 50:3013142008

  • 2

    Alizadeh MPoplawski MMFisher JGorniak RJTDresner AMohamed FB: Zonally magnified oblique multislice and non-zonally magnified oblique multislice DWI of the cervical spinal cord. AJNR Am J Neuroradiol 39:155515612018

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Andre JBBammer R: Advanced diffusion-weighted magnetic resonance imaging techniques of the human spinal cord. Top Magn Reson Imaging 21:3673782010

  • 4

    Atkinson DPorter DAHill DLCalamante FConnelly A: Sampling and reconstruction effects due to motion in diffusion-weighted interleaved echo planar imaging. Magn Reson Med 44:1011092000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Bammer RFazekas F: Diffusion imaging of the human spinal cord and the vertebral column. Top Magn Reson Imaging 14:4614762003

  • 6

    Barakat NMohamed FBHunter LNShah PFaro SHSamdani AF: Diffusion tensor imaging of the normal pediatric spinal cord using an inner field of view echo-planar imaging sequence. AJNR Am J Neuroradiol 33:112711332012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Byun WMShin SOChang YLee SJFinsterbusch JFrahm J: Diffusion-weighted MR imaging of metastatic disease of the spine: assessment of response to therapy. AJNR Am J Neuroradiol 23:9069122002

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Choudhri AFWhitehead MTKlimo P JrMontgomery BKBoop FA: Diffusion tensor imaging to guide surgical planning in intramedullary spinal cord tumors in children. Neuroradiology 56:1691742014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Constantini SMiller DCAllen JCRorke LBFreed DEpstein FJ: Radical excision of intramedullary spinal cord tumors: surgical morbidity and long-term follow-up evaluation in 164 children and young adults. J Neurosurg 93 (2 Suppl):1831932000

    • Search Google Scholar
    • Export Citation
  • 10

    Dowell NGJenkins TMCiccarelli OMiller DHWheeler-Kingshott CA: Contiguous-slice zonally oblique multislice (CO-ZOOM) diffusion tensor imaging: examples of in vivo spinal cord and optic nerve applications. J Magn Reson Imaging 29:4544602009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Fehlings MGMercier D: Factors predicting the resectability of intramedullary spinal cord tumors and the progression-free survival following microsurgical treatment. J Neurosurg Spine 11:5885902009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Gilard VGoia AFerracci FXMarguet FMagne NLanglois O: Spinal meningioma and factors predictive of post-operative deterioration. J Neurooncol 140:49542018

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Grussu FSchneider TZhang HAlexander DCWheeler-Kingshott CA: Neurite orientation dispersion and density imaging of the healthy cervical spinal cord in vivo. Neuroimage 111:5906012015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Huisman TA: Diffusion-weighted and diffusion tensor imaging of the brain, made easy. Cancer Imaging 10 (Spec No A):S163S1712010

  • 15

    Huisman TA: Pediatric tumors of the spine. Cancer Imaging 9 (Spec No A):S45S482009

  • 16

    Jeong EKKim SEGuo JKholmovski EGParker DL: High-resolution DTI with 2D interleaved multislice reduced FOV single-shot diffusion-weighted EPI (2D ss-rFOV-DWEPI). Magn Reson Med 54:157515792005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Leemans AJones DK: The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61:133613492009

  • 18

    Maesawa SFujii MNakahara NWatanabe TWakabayashi TYoshida J: Intraoperative tractography and motor evoked potential (MEP) monitoring in surgery for gliomas around the corticospinal tract. World Neurosurg 74:1531612010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19

    Mansfield POrdidge RJCoxon R: Zonally magnified EPI in real time by NMR. J Phys E Sci Instrum 21:2752801988

  • 20

    Mascalchi MFilippi MFloris RFonda CGasparotti RVillari N: Diffusion-weighted MR of the brain: methodology and clinical application. Radiol Med (Torino) 109:1551972005

    • Search Google Scholar
    • Export Citation
  • 21

    Messiou CCollins DJGiles Sde Bono JSBianchini Dde Souza NM: Assessing response in bone metastases in prostate cancer with diffusion weighted MRI. Eur Radiol 21:216921772011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Pujol SWells WPierpaoli CBrun CGee JCheng G: The DTI challenge: toward standardized evaluation of diffusion tensor imaging tractography for neurosurgery. J Neuroimaging 25:8758822015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Rickert CHPaulus W: Epidemiology of central nervous system tumors in childhood and adolescence based on the new WHO classification. Childs Nerv Syst 17:5035112001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Salmenpera TMSimister RJBartlett PSymms MRBoulby PAFree SL: High-resolution diffusion tensor imaging of the hippocampus in temporal lobe epilepsy. Epilepsy Res 71:1021062006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Samartzis DGillis CCShih PO’Toole JEFessler RG: Intramedullary spinal cord tumors: part I—epidemiology, pathophysiology, and diagnosis. Global Spine J 5:4254352015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Samuel NTetreault LSantaguida CNater AMoayeri NMassicotte EM: Clinical and pathological outcomes after resection of intramedullary spinal cord tumors: a single-institution case series. Neurosurg Focus 41(2):E82016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Saritas EUCunningham CHLee JHHan ETNishimura DG: DWI of the spinal cord with reduced FOV single-shot EPI. Magn Reson Med 60:4684732008

  • 28

    Sąsiadek MJSzewczyk PBladowska J: Application of diffusion tensor imaging (DTI) in pathological changes of the spinal cord. Med Sci Monit 18:RA73RA792012

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29

    Setzer MMurtagh RDMurtagh FREleraky MJain SMarquardt G: Diffusion tensor imaging tractography in patients with intramedullary tumors: comparison with intraoperative findings and value for prediction of tumor resectability. J Neurosurg Spine 13:3713802010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Shibahara ISaito ROsada YKanamori MSonoda YKumabe T: Incidence of initial spinal metastasis in glioblastoma patients and the importance of spinal screening using MRI. J Neurooncol 141:3373452019

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Sofuoğlu OEAbdallah A: Pediatric spinal ependymomas. Med Sci Monit 24:707270892018

  • 32

    Summers PStaempfli PJaermann TKwiecinski SKollias S: A preliminary study of the effects of trigger timing on diffusion tensor imaging of the human spinal cord. AJNR Am J Neuroradiol 27:1952–19612006

    • Search Google Scholar
    • Export Citation
  • 33

    Symms MWheeler-Kingshott CParker GBarker G: Zonally-magnified oblique multislice (ZOOM) EPI in Proceedings of the 8th Meeting of the International Society for Magnetic Resonance in Medicine. Concord, CA: ISMRM2000 p 160

    • Search Google Scholar
    • Export Citation
  • 34

    Sze GBravo SBaierl PShimkin PM: Developing spinal column: gadolinium-enhanced MR imaging. Radiology 180:4975021991

  • 35

    Tartaglino LMFlanders AEVinitski SFriedman DP: Metallic artifacts on MR images of the postoperative spine: reduction with fast spin-echo techniques. Radiology 190:5655691994

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Vargas MIDelavelle JJlassi HRilliet BViallon MBecker CD: Clinical applications of diffusion tensor tractography of the spinal cord. Neuroradiology 50:25292008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Wheeler-Kingshott CAHickman SJParker GJCiccarelli OSymms MRMiller DH: Investigating cervical spinal cord structure using axial diffusion tensor imaging. Neuroimage 16:931022002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Wheeler-Kingshott CAParker GJSymms MRHickman SJTofts PSMiller DH: ADC mapping of the human optic nerve: increased resolution, coverage, and reliability with CSF-suppressed ZOOM-EPI. Magn Reson Med 47:24312002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Wheeler-Kingshott CATrip SASymms MRParker GJBarker GJMiller DH: In vivo diffusion tensor imaging of the human optic nerve: pilot study in normal controls. Magn Reson Med 56:4464512006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Wilm BJSvensson JHenning APruessmann KPBoesiger PKollias SS: Reduced field-of-view MRI using outer volume suppression for spinal cord diffusion imaging. Magn Reson Med 57:6256302007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Xu DMori SSolaiyappan Mvan Zijl PCDavatzikos C: A framework for callosal fiber distribution analysis. Neuroimage 17:113111432002

  • 42

    Xue YHauskrecht M: Active learning of classification models with Likert-scale feedback. Proc SIAM Int Conf Data Min 2017:28352017

  • 43

    Yeom KWHoldsworth SJVan ATIv MSkare SLober RM: Comparison of readout-segmented echo-planar imaging (EPI) and single-shot EPI in clinical application of diffusion-weighted imaging of the pediatric brain. AJR Am J Roentgenol 200:W437432013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Zhang L: Convergence and stability of the exponential Euler method for semi-linear stochastic delay differential equations. J Inequal Appl 2017:2492017

    • Search Google Scholar
    • Export Citation
  • 45

    Zhang YDZhu FPXu XWang QWu CJLiu XS: Classifying CT/MR findings in patients with suspicion of hepatocellular carcinoma: comparison of liver imaging reporting and data system and criteria-free Likert scale reporting models. J Magn Reson Imaging 43:3733832016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

TrendMD

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 85 85 36
Full Text Views 21 21 14
PDF Downloads 9 9 4
EPUB Downloads 0 0 0

PubMed

Google Scholar