Artefacts and diagnostic pitfalls in PETMRI

RAD Magazine, 42, 499, 12-13 Design of current PETMRI scanners Andrew Mallia Although PETCT and stand-alone MRI are well-established Clinical research fellow, Cancer Imaging Department and imaging modalities, the combination of PET and MRI in one device resulted from significant hardware and software engi- King’s College London and Guy’s and St Thomas’ PET neering developments. Fully integrated PETMRI systems Centre, Division of Imaging Sciences and Biomedical are now commercially available. In these systems, the PET Engineering, King’s College London detector ring is inserted into the MRI system allowing simul- [email protected] taneous data acquisition of PET and MRI at the same bed position. Gary Cook For this to be possible the photomultiplier tubes (PMT) were replaced by avalanche photodiodes (APDs) or silicon Head of cancer imaging, Cancer Imaging Department and PMTs and shielding had to be adjusted to allow for the PET King’s College London and Guy’s and St Thomas’ PET electronics to operate in the presence of rapidly changing Centre, Division of Imaging Sciences and Biomedical gradient fields. With such detector technology, PET and MRI Engineering, King’s College London; honorary consultant in acquisitions can occur simultaneously, rather than sequen- nuclear medicine, Guy’s and St Thomas’ NHS tially as with PETCT. Using these simultaneous systems minimises misregistration from patient motion and allows Foundation Trust the physiological effects and functional parameters of the Vicky Goh two components to be matched in time (figure 2).3 Chair of clinical cancer imaging, Cancer Imaging Attenuation correction methods Department, Division of Imaging Sciences and Biomedical In PETCT, information on tissue specific photon attenuation Engineering, King’s College London; honorary consultant that is required for PET data correction is derived from the radiologist, Guy’s and St Thomas’ NHS Foundation Trust CT data. The most common approach is to use a bilinear relationship to convert the CT Hounsfield Units values to Radhouene Neji linear attenuation coefficients for 511keV photons. This is MR collaboration scientist, Siemens Healthcare Limited, UK done on a voxel-by-voxel basis without the need for tissue segmentation. The resulting image is referred to as an atten- Jane Mackewn uation correction map. Medical physicist, King’s College London and Guy’s and The AC in PETMRI systems is based on MRI data, which are related to water and fat content (proton density) rather St Thomas’ PET Centre than photon attenuation, so there is no simple relation James Stirling between MRI signal intensity and attenuation coefficients. The MRI signal depends on protons and their local environ- PETMRI superintendent, King’s College London and ment, whereas photon attenuation in PET depends on elec- Guy’s and St Thomas’ PET Centre tron density and atomic number. Determining photon attenuation from MR data is therefore challenging and not Sami Jeljeli fully resolved. PET radiographer, King’s College London and Guy’s and One solution is to acquire a two-point Dixon volume-inter- St Thomas’ PET Centre polated 3D breath-hold sequence and the post processed information it provides is used to derive an attenuation map (µ-map) based on four tissue types: air, lung, soft tissue and fat. Linear attenuation coefficients representative of such tissue types are then assigned to these regions.5 Bone has Introduction a low MR signal, therefore it appears dark with a similar PETMRI has recently been introduced into clini- intensity to air and is not represented in the MR AC map. This can potentially lead to quantitative inaccuracies in AC cal practice. It maximises diagnostic information PETMRI images with under-estimation of tracer uptake.1,2 by unifying the excellent anatomical morpholog- So far no studies comparing PETCT and PETMRI report ical and functional information available from undetected bone lesions on PETMRI, despite an underesti- MRI and the molecular and metabolic informa- mation of the standardised uptake value (SUV). Bone, unlike tion from PET (figure 1).1 air, produces a signal that can be collected by an ultra-short echo time (UTE) sequence, allowing it to be included as an PETMRI is currently one of the most active additional class.6 UTE sequences are currently used for AC areas of research in diagnostic imaging, and correction of brain PETMRI studies. Other less commonly areas where this modality can bring potential used methods for AC in PETMRI include: 1) atlas and benefits in clinical practice are being machine learning based methods which deform an atlas or investigated.2 This review briefly describes the a template to morph it to the patient’s MR image and obtain an attenuation map, and 2) methods which exploit the PET design of PETMRI scanners, including attenua- emission data and anatomical information from MR images tion correction (AC) methods that are essential to compute the attenuation maps. for PET data accuracy, and addresses some of the most common artefacts and pitfalls encountered Pitfalls/artefacts with PETMRI. Every new imaging modality introduces new types of arte- facts. Apart from having an effect on the visual impression of either PET or MR data, artefacts in PETMRI can affect magnetic interfaces result in local geometric distortions and both PET and MR quantification analysis. These include lack of fat suppression. The introduction of higher magnetic artefacts related to the reduced field of view of MRI com- field strengths into clinical use has the advantage of increas- pared to PET (truncation artefacts), dental and orthopaedic ing the signal (which can be used in producing higher qual- hardware, inaccurate bone tissue segmentation, fat/water ity images) but has the disadvantage of increasing the swapping, echo planar imaging-based distortion artefacts inhomgeneity of the magnetic field within the bore of the and artefacts that are accentuated at 3.0T, the magnetic scanner. Field inhomogeneity produces blurring, distortion field strength of current commercial PETMRI systems. and signal loss at tissue interfaces, particularly at the edge of the field of view (figure 4).1 Truncation artefacts Geometric distortions in DWI secondary to eddy currents These are an imaging effect where there is lack of signal can also occur. Eddy currents are loops of electric current from body parts outside a given field of view (FOV) for one induced within conductors by a changing magnetic field in of the modalities of a hybrid imaging method. This leads to the conductor. Eddy currents can originate in any conductive an abrupt cut off of the body structures in the periphery of part of the MRI scanner (cryostat, RF coils). The magnitude the image, typically laterally. In PETCT an underestimation of the current is proportional to the strength of the magnetic of radioactivity in the truncated area can occur and lesions field. Eddy currents create magnetic field variations that with increased tracer uptake may not be represented ade- can result in geometric distortions in the DWI images. quately. Some PETCT scanners generate a separate non- Several patterns have been recognised such as contraction diagnostic CT image with extended FOV to improve PET or dilation of the image and overall shift.9 Figure 4 shows quantitative accuracy. an example in which an overall shift occurred which could Truncation artefacts in PETMRI occur because the actual have potentially led to an incorrect anatomical correlation. FOV in MRI is smaller than the FOV in PET. These imag- These types of distortions can be detected by comparing the ing artefacts are frequently seen in large patients, when DWI images with artefact-free anatomical T1 or T2 images. patients are scanned with their arms down and when patients are positioned away from the in-plane centre. Accentuated 3.0T artefacts Truncation artefacts also occur due to the inherent inhomo- Susceptibility and standing wave effects may result in ‘dark geneity of the main static field and the non-linearity of the holes’ (figure 5). Magnetic susceptibility is the extent to applied magnetic field gradients, which degrades with which a material becomes magnetised when placed in a increasing distance to the isocentre. magnetic field and can be caused by metallic objects or in regions close to gas-filled structures. Standing wave effects Dental artefacts are more significant at 3.0T and are related to the higher Metal dental implants can be made out of different materials frequency of the B1 transmit field (RF pulse) resulting in and are often unpredictable. A signal void on the MR AC strong signal variations across an image. map at the level of the mandible without any associated abnormal uptake on the fused PETMRI images is often Conclusion noted. These artefacts are normally associated with an over- PETMRI’s clinical applications are bound to increase in the estimation of the activity on the PETCT images.1 coming years, involving the fields of oncology, neurology and cardiovascular imaging. Fat/water swaps Clinicians reporting PETMRI studies should develop a Although Dixon methods are widely used due to recent technical understanding of the underlying mechanisms caus- developments, they still have their limitations. An artefact ing these artefacts, otherwise these can be misleading for occasionally occurs wherein the reconstruction will produce the diagnosis. Review of both the AC and non-AC images a fat-only image when a water-only image is desired. In the together with the MR images and the MR-based attenuation case of PETMRI fat/water swaps may occur in the AC and maps can help detect potential artefacts/pitfalls arising from diagnostic T1 dual echo Dixon sequences as well as the cor- MR AC. responding MR AC maps. The exact impact of these arte- facts in PETMRI is not yet known, but there are some References studies suggesting that those occurring in the AC DIXON 1, Martinez-Rios C, Muzic R F, DiFilippo F P et al. Artefacts and diagnostic sequences can cause a 20% change in the SUVs when com- pitfalls in positron emission tomography-magnetic resonance imaging. 8 Semin Roentgenol 2014;49(3):255-70. pared to the PETCT of the same patient. In our early expe- 2, Kuwert T, Ritt P. PET/MRI and PET/CT: Is there room for both at the rience with PETMRI we have not noticed any major top of the food chain? Eur J Nucl Med Mol Imaging 2016;43(2):209-11. differences in SUVs (in areas with fat/water swaps) that can 3, Torigian D A, Zaidi H, Kwee T C et al. PET/MRI imaging: Technical have a significant clinical impact. However, it is important aspects and potential clinical applications. Radiology 2013;267:26-44. 4, MAGNETOM Flash, The Magazine of MR. ISMRM edition 2011;1:102. to review the MR AC images for identification of fat/water 5, Boellaard R, Quick H H. Current image acquisition options in PET/MR. swap artefacts that might impact the AC map (figure 3). Semin Nucl Med 2015;45(3):192-200. 6, Berker Y, Franke J, Salomon A et al. MRI-based attenuation correction Echo planar imaging (EPI) artefacts for hybrid PET/MRI systems: A 4-class tissue segmentation technique using a combined ultra-short-echo-time/Dixon MRI sequence. J Nucl Med EPI is a fast imaging method used for diffusion-weighted 2012;53:796-804. imaging (DWI) that acquires multiple k-space lines following 7, Keller S H, Holm S, Hansen A E et al. Image artefacts from MR-based a single excitation. DWI is being increasingly used in onco- attenuation correction in clinical, whole-body PET/MRI. Magn Reson logical imaging, since it can help differentiate malignant Mater Phy 2013;26:173-81. 8, Ladefoged C N, Hansen A E, Keller S H et al. Impact of incorrect tissue from benign lesions and tumours from oedema and classification in Dixon-based MR- AC: Fat-water tissue inversion. Eur J infarction. Nucl Med Mol Imaging Physics 2014;1:101. Distortion artefacts are commonly noted in DWI images 9, Le Bihan D, Poupon C, Amadon A et al. Artefacts and pitfalls in diffusion as a result of the k-space lines being acquired in a single MRI. J Magn Reson Imaging 2006;24:478-88. 10, Merkle M A, Dale M B. Abdominal MRI at 3.0T: The basics revisited. Am train and rapid gradient switching during the acquisition. J Roentgenol 2006;186(6):1524-32. A source of distortion includes inhomogeneity of the static magnetic field (B0) and high magnetic susceptibility. EPI requires a very homogeneous magnetic field, and ABCD A BC

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Figure 1 Figure 3 F-18 FDG and C-11 methionine PETMRI in a patient (A) Normal PETMRI µ-map. (B) PETMRI µ-map in with a low grade left hemispheric glioma: (A) high which fat (dark grey pixels, green dot) and water tissue contrast is obtained using a T1W 3D isotropic (light grey pixels, blue dot) have been swapped in MP-RAGE sequence; (B) axial T2W fluid suppressing the brain (red brackets). (C) PETMRI µ-map in sequence (FLAIR); (C) ADC (shows cellular density); which fat (dark grey pixels, green dot) and water (D) MR spectroscopy is used to map out different (light grey pixels, blue dot) have been swapped in metabolites; (E) axial F-18 FDG PET images (shows the head/neck and abdominal regions (red brackets). glucose metabolism); (F) axial fused T2W/F-18 FDG Fat/water swaps can cause changes in calculation of PET; (G) axial C-11 methionine PET images (shows SUVs. (Courtesy of the PET Centre, St Thomas’ Hospital.) amino acid metabolism); (H) axial fused T2 flair/C-11 methionine. (Courtesy of the PET Centre, St Thomas’ Hospital.) ABC

A LSO array

Crystals Avalanche photo diodes (APD) 3x3 APD array Integrated ABC 9-channel cooling preamplifier channels ASIC board 9-channel driver board

B Magnet shielding coil Primary magnet coil Figure 4 Gradient coil Top row: (A) Localised distortion artefact (yellow PET detector arrow) on the axial DWI imaging in a patient with a RF body coil primary right lung cancer. This occurs as a result of Magnet cryostat magnetic field (B0) inhomogeneity away from the isocentre. (B,C) Primary right lung cancer (red arrows) shown on axial T1 weighted and fused PETMRI images. Bottom row: Geometric distortion with the fused T1 DWI high b value which arises from EPI sequences for diffusion imaging. (A,B) The high intensity signal within a right retrocrural lymph node (red arrows) has been (C) displaced posteriorly into the adjacent thoracic vertebra on the fused T1 DWI high b value image (yellow Figure 2 arrow). (Courtesy of the PET Centre, St Thomas’ Hospital.) Example of a PET detector assembly on the Biograph mMR (Siemens Healthcare, Erlangen, AB Germany.4 (A) Lutetium oxyorthosilicate (LSO) crys- tals create light events from 511keV gamma rays which are detected by a 3 x 3 array of avalanche photo diodes (ADP). This type of design is free of magnetic components and is able to perform in strong magnetic fields. (B) Integration of the PET detectors in the MRI hardware. From the inside to outside: RF body coil, PET detector, gradient coil assembly, primary magnetic coil, and magnetic shielding coil. The PETMRI integration requires Figure 5 that the PET detector works within strong static ‘Dark holes’ (yellow arrows) resulting from (A) sus- and dynamic magnetic field and does not disturb ceptibility artefacts and (B) standing wave effects. any of the associated electromagnetic MR fields. (Courtesy of the PET Centre, St Thomas’ Hospital.)