Multiparametric Mri Tissue Characterization Essay

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Review

PET/MRI in Oncological Imaging: State of the Art

Usman Bashir 1, Andrew Mallia 1, James Stirling 1,2, John Joemon 2, Jane MacKewn 2, Geoff Charles-Edwards 1,3, Vicky Goh 1,4 and Gary J. Cook 1,2,*

1

Cancer Imaging Department, Division of Imaging Sciences and Biomedical Engineering, King’s College London, London, SE1 7EH, UK

2

PET Imaging Centre and the Division of Imaging Sciences and Biomedical Engineering, King’s College London, London, SE1 7EH, UK

3

Medical Physics, Guy’s & St Thomas’ Hospitals NHS Foundation Trust, London, SE1 7EH, UK

4

Department of Radiology, Guy’s & St Thomas’ Hospitals NHS Foundation Trust, London, SE1 7EH, UK

Academic Editor: Andreas Kjaer

Received: 16 June 2015 / Accepted: 10 July 2015 / Published: 21 July 2015

Abstract

: Positron emission tomography (PET) combined with magnetic resonance imaging (MRI) is a hybrid technology which has recently gained interest as a potential cancer imaging tool. Compared with CT, MRI is advantageous due to its lack of ionizing radiation, superior soft-tissue contrast resolution, and wider range of acquisition sequences. Several studies have shown PET/MRI to be equivalent to PET/CT in most oncological applications, possibly superior in certain body parts, e.g., head and neck, pelvis, and in certain situations, e.g., cancer recurrence. This review will update the readers on recent advances in PET/MRI technology and review key literature, while highlighting the strengths and weaknesses of PET/MRI in cancer imaging.

*

Author to whom correspondence should be addressed; Tel.: +44-207-188-8364; Fax: +44-207-620-0790.

Keywords:

PET/MRI; MR-PET; cancer; diagnosis; imaging

1. Introduction

Combined positron emission tomography with magnetic resonance imaging (PET/MRI) is a promising new modality which may replace PET/CT in selected cancer scenarios and may generate new oncological applications. In PET/CT, the limited spatial resolution of PET is compensated by CT, providing valuable anatomic and morphological information complementary to the metabolic and molecular information provided by PET, making it a mainstay investigation in staging and re-staging of a wide range of cancers [1]. Some of the issues in PET/CT include the added radiation dose from CT and the limited soft-tissue contrast resolution of CT. MRI, however, not only offers superior contrast resolution between different types of soft tissues, it allows physiological (e.g., dynamic contrast enhanced MRI), metabolic (e.g., MR spectroscopy), and molecular (e.g., diffusion weighted imaging) phenomena to be observed. Based on these advantages, it would be expected that hybrid PET/MRI scanners may provide a superior solution to PET/CT in some cancer imaging applications.

Although PET/MRI has been investigational since before PET/CT, several technological problems have prevented its clinical deployment [2,3,4]. First, physically combining the two scanner types has been a challenge for a number of reasons. For example: (a) conventional photomultiplier tubes used in standard PET detectors are highly sensitive to even relatively small magnetic fields and therefore cannot be located in or even near to an MRI scanner; (b) Radiofrequency (RF) cross talk can occur between the two scanners in the absence of appropriate RF shielding; and (c) there is only a limited amount of available space inside an MR scanner in which a PET ring can be located, when considering a fully integrated system. Second, attenuation correction, which is an essential part of PET imaging and is performed using the CT data on conventional PET/CT platforms, is more complicated using an MRI image as the image intensity bears no direct relationship to tissue attenuation. Methods instead rely on tissue segmentation, i.e., deriving different classes of tissue type which are then assigned to a particular attenuation factor, or Atlas based approaches.

Recent advances in engineering have addressed these issues to a large extent, and studies are underway to assess the effectiveness of PET/MRI, compared with PET/CT. Most studies indicate that cancer staging with PET/MRI is feasible and as accurate as PET/CT in most body regions; in head, neck, and pelvis, there is evidence that PET/MRI may be superior to PET/CT. A second question which is being pursued is the logistical advantage in combining PET and MRI into a single examination in situations when both are commonly performed, for example, in relapse of pelvic malignancies. In such situations there may be advantages in patient-experience, reduced radiation and cost-saving. Therefore, the purpose of this review is to:

  • Provide an overview of the technical aspects of PET/MRI design.

  • Describe the limitations of simultaneous PET/MRI imaging.

  • Review current literature investigating the diagnostic accuracy of PET/MRI in cancer imaging compared with the conventional imaging tools, in particular, PET/CT. By order of preference, recent studies utilizing hybrid PET/MRI scanners will be mentioned before studies performed on fused PET and MRI data acquired separately.

2. Technical Aspects of PET/MRI

Although first experiments on PET/MRI started earlier than PET/CT, in the mid-1990s [5], clinical implementation has lagged behind PET/CT due to the greater number of technological challenges that have had to be addressed. Various PET/MRI designs have been investigated over recent years that address the issues outlined in Section 1 above. Second, attenuation correction, an essential part of any PET platform, is not as robust with PET/MRI as it is with PET/CT [6]. The following paragraphs will discuss both technical aspects of PET/MRI imaging in turn:

2.2. Sequential

A sequential design involves imaging on separate PET and MRI systems. The PET and MRI units may be in the same room (e.g., Phillips Ingenuity TF PET/MR) or in separate rooms (e.g., GE trimodality PET/CT/MRI). The patient remains on a mobile scanning couch and is transferred from one scanner to the other and, therefore, spatially co-registered images are acquired without the need to reposition the patient.

A sequential PET and MRI setup is the technologically least challenging and economical solution, albeit with its limitations, i.e., greater space requirements to house two separate scanners (typically 4.3 × 13 m), increased time required for two separate acquisitions, and propensity for artefact as the patient may move between acquisitions [7].

2.3. Simultaneous

Scanners which perform PET and MRI simultaneously have been in use since 2006 [8,9,10]. However, combining PET and MRI detectors into a single gantry is, technically, the most challenging design requiring all issues described in Section I to be fully addressed. Designs of such systems include placing the PMTs at a distance from the magnetic field via long optic fibers in preclinical scanners [11], using an MR magnet with a gap housing PET detectors (“split design concept”), and more recently, using field insensitive solid-state detectors—the avalanche photo-diodes (APD)—in place of PMTs. PET/MRI scanners utilizing APD detectors in a fully-integrated PET/MRI assembly have shown promising diagnostic quality. However, these scanners do not allow time-of-flight (TOF) PET due to the low timing resolution of APD detectors. More recently, PET/MR models utilizing silicon photomultiplier tubes (SiPMT) in place of APDs have become available. These scanners are TOF-enabled because of the high timing resolution of SiPMTs.

Interested readers are pointed to the following reviews for further technological and historical details on the development of PET/MR [7,12].

2.4. Attenuation Correction in PET/MRI

In PET imaging, the radionuclide decays and results in the emission of two annihilation photons of 511 keV in opposite directions, along a “line of response” (LOR). Opposing PET detectors are linked to register co-incident counts as a single event. However, one or both photons from a single event may be attenuated by body tissues before being detected, causing loss of signal proportional to the depth of the annihilation event from surface and regional tissue density. Attenuation correction (AC) is a post-processing step which accounts for these attenuation variations and is essential in providing PET images of diagnostic quality and quantitative accuracy.

The present solution of CT-based transmission systems as used in PET/CT attenuation correction is not possible in PET/MRI. This is because CT measures photon attenuation and, being similar in principle to PET, allows attenuation correction of the higher energy (511 keV) gamma photons. MRI, conversely, measures signals based on proton density and is unable to provide an analogous AC to CT. Several “work-around” solutions have been devised to allow MRI-based AC, and can be broadly classified into software based AC algorithms and dedicated AC sequences. For the sake of simplification, a generalized overview of the various approaches is provided below; interested readers are referred elsewhere[13].

Software-based algorithms: These approaches derive AC maps for patient datasets either through the use of template data-sets or artificial intelligence algorithms. Techniques relying on templates utilize pre-available templates of normal MRI and co-registered CT-derived attenuation maps. A patient MRI scan is matched with the template MRI to generate a patient-specific mathematical transformation. This transformation is then applied to the template attenuation map to derive a patient-specific attenuation map. The utility of template-based AC is limited to brain imaging. Artificial intelligence (AI) techniques, however, do not require templates, and process patient-images to segment anatomical structures such as brain, sinuses, and bone with the help of AI algorithms (e.g., fuzzy logic and neural networks). AI techniques can be utilized in whole body imaging and are considered superior to template-based approaches.

AC-specific sequences: These sequences are usually acquired before diagnostic sequences. 2-point Dixon volume-interpolated breath-hold examination (VIBE) sequences are fast and allow derivation of an attenuation map based on four tissue-types: air, lungs, soft-tissue, and fat. However, due to the signal void within cortical bone, bone attenuation is also categorized as soft-tissue and this may lead to underestimations of SUVs in bone lesions by as much as 30% [3,14,15] (Figure 1). Despite the imperfect AC in the current MRI-based AC techniques, several in vivo studies on patients have not shown a significant disadvantage in detection of lesions [16,17]. Nevertheless, alternative approaches utilizing ultra-short TE MR sequences may allow improved profiling of bone attenuation, although such approaches have their own limitations—artifacts at larger FOV and extra acquisition time [18].

Figure 1. (A) Coronal plane image from the Dixon VIBE sequence used to generate a MR AC map; (B) shows attenuation map generated from (A). Note four gray levels separating air, lung, fat, and soft-tissue. Also note that while bone marrow appears similar to fat elsewhere, bone cortex and overlying muscles have been assigned similar attenuation values. Reliable separation of bone in AC maps is an area of active research; (C) A non-corrected 18F-FDG PET image, showing non-uniform tracer distribution with spuriously higher uptake in peripheral tissues due to greater attenuation of emission photons from deeper structure; (D) AC-corrected image after applying MRI-based attenuation map shown in (B).

Figure 1. (A) Coronal plane image from the Dixon VIBE sequence used to generate a MR AC map; (B) shows attenuation map generated from (A). Note four gray levels separating air, lung, fat, and soft-tissue. Also note that while bone marrow appears similar to fat elsewhere, bone cortex and overlying muscles have been assigned similar attenuation values. Reliable separation of bone in AC maps is an area of active research; (C) A non-corrected 18F-FDG PET image, showing non-uniform tracer distribution with spuriously higher uptake in peripheral tissues due to greater attenuation of emission photons from deeper structure; (D) AC-corrected image after applying MRI-based attenuation map shown in (B).

3. Imaging Protocols and Workflow

Sequential PET/MRI involves longer scan acquisition times compared to simultaneous PET/MRI since the patient is imaged twice, once with PET, and once with MRI. Here, we present an overview of simultaneous PET/MRI workflow based on our experience.

Patient preparation for PET/MRI accounts for the contraindications and precautions for both modalities. Hence, as for 18F-fluorodeoxyglucose (18F-FDG) PET in PET/CT, the requirements include a four-hour fast, control of blood glucose level, and having the patient rest after FDG injection, to minimize muscle uptake. The contraindications to PET/MRI are the same as for MRI, e.g., checks for metallic implants and pacemakers, and for PET, e.g., pregnancy.

Patient positioning for PET/MRI needs to be more precise than is necessary for PET, especially with regards to patient centering on the imaging couch and positioning of the surface coils, to optimize the MRI-image signal and avoid artifacts. Hence, positioning takes longer than it does for routine PET, and can potentially add to staff radiation. Therefore, staff should preferentially be trained in both PET and MRI.

Once the patient has been positioned, an MRI localizer sequence (analogous to scout scan in CT) is acquired to determine scan range. Thereafter, PET acquisition is straightforward, requiring input of the number of bed positions and time at each bed position (typically 3–4 min but can be extended to make use of the longer MRI scan-time). Concurrent to PET acquisition, an MRI attenuation correction sequence (2-point Dixon VIBE) is acquired, followed by the diagnostic MRI sequences for the current bed position. A number of diagnostic MRI sequences may be selected and can be varied flexibly according to body region and clinical question, but usually at a minimum include a T1-weighted and a T2-weighted sequence[19]. A typical PET/MRI workflow is illustrated in Figure 2.

Figure 2. A typical PET/MRI workflow, as performed in our institution. Patients are scanned in four bed positions to cover the anatomy from head to mid-thighs. Whole body imaging is performed first, followed by targeted sequences for the region of interest. Typically, a scan lasts for 60 min.

Figure 2. A typical PET/MRI workflow, as performed in our institution. Patients are scanned in four bed positions to cover the anatomy from head to mid-thighs. Whole body imaging is performed first, followed by targeted sequences for the region of interest. Typically, a scan lasts for 60 min.

A “minimalist” PET/MRI protocol including only 2-point Dixon VIBE for both AC and anatomic localization has been validated and takes less than 20 min [17]. On the other hand, a typical whole body study including organ-targeted sequences can easily take 60-min or more, compared with about 15–30 min typical for PET/CT. The longer time required to perform PET/MRI is an important issue and will result in costlier studies compared with PET/CT, which must be borne in mind while justifying its financial feasibility in clinical settings [19,20].

4. Overview of Cancer Imaging

PET/MRI is expected to supersede PET/CT in imaging cancers which are anatomically better defined by MRI compared to CT, due to its superior soft-tissue contrast. These include brain, head and neck, breast, liver, musculoskeletal system, and urogenital tumors [21]. New applications, not addressed by CT, may also become apparent. For example, MRI sequences for the measurement of tumor perfusion (i.e., dynamic contrast-enhanced MRI or arterial spin labelling) and hypoxia (e.g., blood-oxygen-level-dependent “BOLD-MRI”) may be used independently or to cross-validate PET tracers for similar purposes, such as 15O-H2O (perfusion) or 18F-fluoromisonidazole (hypoxia). Complementary data from PET tracers and MRI sequences designed to answer similar questions may provide additional information. Given below is an overview of the current literature on applications of PET/MRI divided into three sections: organ-based assessment of local tumor, detection of lymph node metastases, and detection of distant metastases.

5. Assessment of Local Tumor

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