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PET/MRI

Posted Jan 31, 2016 Updated Apr 10, 2023
By Tyler J. Fraum MD , Kathryn J. Fowler MD , Jonathan McConathy MD PhD
25 min read

Positron emission tomography (PET), commonly performed in conjunction with computed tomography (CT), has revolutionized oncologic imaging. PET/CT has become the standard of care for the initial staging and assessment of treatment response for many different malignancies. Despite this success, PET/CT is often supplemented by magnetic resonance imaging (MRI), which offers superior soft-tissue contrast and a means of assessing cellular density with diffusion-weighted imaging. Consequently, PET/MRI, the newest clinical hybrid imaging modality, has the potential to provide added value over PET/CT or MRI alone. The purpose of this article is to provide a comprehensive review of the current body of literature pertaining to the clinical performance of PET/MRI, with the aim of summarizing current evidence and identifying gaps in knowledge to direct clinical expansion and future research. Multiple example cases are also provided to illustrate the central findings of these publications.

Introduction

Positron emission tomography (PET) has revolutionized the imaging evaluation of numerous oncologic conditions by exploiting biochemical and physiologic differences between tumor cells and normal tissues . Often performed in conjunction with computed tomography (CT), PET utilizing the glucose analog 2-deoxy-2-[ 18 F]fluoro-D-glucose (FDG) has become the standard of care for the initial staging and the subsequent assessment of treatment response for many malignancies . Tumor uptake of FDG reflects the increased rates of aerobic glycolysis that occur in many cancer cells (the Warburg effect) relative to most normal tissues and benign lesions. The resulting distribution of FDG thereby allows for anatomic delineation of local and distant tumor spread by PET/CT and provides a measure of a key aspect of cancer metabolism. Many PET tracers have also been developed to take advantage of other distinctive tumor properties, such as elevated amino acid transport or altered receptor expression .

Despite its proven utility, FDG-PET/CT has important limitations, especially with respect to local tumor staging and the characterization of certain incidental lesions. In such situations, further evaluation with magnetic resonance imaging (MRI) may be indicated to achieve optimal clinical management. The superb soft-tissue contrast of MRI and its capacity to assess cellular density by diffusion-weighted imaging (DWI) constitute powerful supplements to the molecular and metabolic data of PET. Consequently, PET/MRI, the newest clinical hybrid imaging modality, has significant potential to improve the diagnosis, initial staging, and subsequent restaging of numerous cancers. However, studies demonstrating such benefits are needed to support the routine clinical use of PET/MRI, particularly to justify the added expense and complexity of PET/MRI instead of PET/CT. This review aims to summarize the current body of evidence in support of PET/MRI, as well as current challenges and gaps in knowledge, and to identify oncologic conditions likely to benefit from its clinical use. We also present case examples to illustrate specific advantages of PET/MRI. Overall, this article should familiarize the reader with the current clinical applications of PET/MRI in oncology and provide an overview of the specific scenarios in which PET/MRI may provide added value over PET/CT or MRI alone.

Current Challenges

Technical Considerations

Before delving into the clinical evidence, it is essential to discuss briefly the technical development of PET/MRI, so as to understand some of the inherent advantages, challenges, and limitations. The earliest approach to combining PET and MRI data was through software fusion of PET or PET/CT images with separately acquired MRI. The first combined apparatuses were sequential PET/MRI systems that consisted of individual PET and MRI elements connected by a common table. The newer integrated PET/MRI systems acquire PET and MRI data simultaneously in the same bore. This latter strategy may improve scanning efficiency and reduce misregistration but requires technical adaptations of the PET components; additionally, both sequential and integrated PET/MRI systems require a novel method to correct for the attenuation of PET photons .

Whereas the CT component of PET/CT directly provides electron density information that can be readily used to generate attenuation-corrected PET images, the MRI signal acquired during simultaneous PET/MRI instead correlates with proton density and tissue T1/T2 properties. Current approaches to MRI-based attenuation correction (AC) include segmentation-based and atlas-based methods . Segmentation-based AC is used clinically and relies on the Dixon method to classify voxels as soft tissue (i.e., muscle and solid organs), fat, lung, or air. In contrast to the atlas-based method, which fits pre-existing averaged imaging data sets to an acquired study and is currently used mainly in the research setting, the segmentation-based method uses each patient’s own imaging data and thus can account for large tumors, postsurgical changes, anatomic variants, and other findings not readily incorporated into imaging atlases. However, segmentation-based AC has its own set of limitations. Cortical bone, which attenuates PET photons more than soft tissue, does not provide adequate signal to be represented in AC maps derived from the current clinically available MRI-based segmentation methods. Consequently, cortical bone is not accounted for by the standard Dixon method, resulting in lower standardized uptake values (SUVs) for tissues within or immediately adjacent to cortical bone when assessed by PET/MRI compared to PET/CT . Segmentation of the lung parenchyma can occasionally fail due to the relative lack of protons available to provide MR signal compared to fat or soft tissue, resulting in artifacts that propagate into the attenuation-corrected PET images and may compromise interpretation . Additionally, patient-positioning devices, such as the headphones routinely used in brain MRI, can also artifactually lower SUVs derived from MR-based AC methods . In general, compared to CT-based AC, the maximum reductions in SUV measurements derived from MR-based AC are typically on the order of 10–20%, although the diagnostic impact of this SUV underestimation on routine clinical oncologic imaging with PET/MRI appears to be relatively minor.

Workflow Optimization and Protocol Design

Given the relative novelty of PET/MRI, no standardized acquisition protocols exist. This protocol variability throughout the PET/MRI literature can make comparing the results of different studies challenging. Importantly, protocol optimization and sequence selection have been extensively described in the literature ( Table 1 ). Regardless of the acquisition details, there are basic principles that should apply to clinical protocol development: (1) PET/MRI protocols should be designed to compete with PET/CT in terms of examination duration, and (2) PET/MRI protocols should be tailored to the clinical question at hand, with the goal of creating added value beyond what PET/CT or MRI alone might otherwise provide. At our institution, initial staging studies generally include both whole-body sequences aimed at identifying distant metastases and high-resolution, anatomically focused MR sequences in the region of the primary tumor to facilitate assessment of local invasion and detection of regional metastases.

TABLE 1

Publications Addressing PET/MRI Workflow Considerations, Protocol Design, and Sequence Optimization

Fowler et al. Whole-body simultaneous positron emission tomography (PET)-MR: optimization and adaptation of MRI sequences . Von Schulthess et al. Workflow considerations in PET/MR imaging . Vargas et al. Approaches for the optimization of MR protocols in clinical hybrid PET/MRI studies . Barbosa et al. Workflow in simultaneous PET/MRI . Martinez-Möller et al. Workflow and scan protocol considerations for integrated whole-body PET/MRI in oncology . Kalemis et al. Sequential whole-body PET/MR scanner: concept, clinical use, and optimization after two years in the clinic. The manufacturer’s perspective . Reiner et al. Protocol requirements and diagnostic value of PET/MR imaging for liver metastasis detection .

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Economic Considerations

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Emerging Clinical Applications and Evidence

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Whole-body Staging

Comparing PET/MRI to PET/CT

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Figure 1, 29-year-old woman with newly diagnosed cervical cancer presented for initial staging. Coronal T2-weighted images (T2WIs) with 2-deoxy-2-[ 18 F]fluoro-D-glucose-positron emission tomography (FDG-PET) fusion ( a posterior to b ) revealed marked tracer uptake by an infiltrative mass ( arrow ) just inferior to the uterus ( arrowhead ) and posterior to the urinary bladder ( asterisk ), compatible with the patient's known cervical cancer. There was no evidence of pelvic nodal disease or distant metastases. This case highlights the potential of PET/magnetic resonance imaging (MRI) to serve as a whole-body imaging modality for multiple oncologic indications. (Color version of figure available online.)

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Figure 2, 69-year-old man with known metastatic papillary thyroid carcinoma presented for restaging. Sagittal computed tomography (CT) images (a) revealed a subtle lytic lesion within the T2 vertebral body ( arrow head ) but a normal appearance of the T5 vertebral body ( arrow ). Sagittal CT images with 2-deoxy-2-[ 18 F]fluoro-D-glucose-positron emission tomography (FDG-PET) fusion (b) demonstrated an FDG-avid focus in the T2 ( arrowhead ) vertebral body highly suspicious for metastatic disease. In contrast, a focus of more subtly increased FDG uptake in the T5 vertebral body ( arrow ) without a CT correlate was felt to be indeterminate, as both metastatic disease and degenerative disease could conceivably produce this appearance. Sagittal T1-weighted images (T1WIs) (c) from subsequent PET/magnetic resonance imaging (MRI) showed clear evidence of marrow replacement in the T2 ( arrowhead ) and T5 ( arrow ) vertebral bodies. Corresponding foci of FDG avidity on sagittal T1WIs with FDG-PET fusion (d) strongly supported the presence of metastases at both sites. These images show an example of the improved anatomic delineation of malignant osseous disease with PET/MRI relative to PET/CT, as well as the power of PET/MRI to distinguish osseous malignancy from degenerative remodeling. (Color version of figure available online.)

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Radiation Reduction

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Specific Indications

Intracranial Neoplasms

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Figure 3, 8-year-old girl with suspected recurrent small cell glioma presented for restaging. (a) Transaxial contrast-enhanced T1-weighted images (T1WIs) showed a heterogeneous mass ( arrows ) centered in the right basal ganglia. Multiple small nonenhancing areas ( asterisks ) interspersed among numerous enhancing foci were noted. (b) Transaxial contrast-enhanced T1WIs with 6-[ 18 F]fluoro-3,4-dihydroxy-phenylalanine-positron emission tomography (FDOPA-PET) fusion revealed avid tracer uptake by the enhancing and nonenhancing portions of this mass ( arrows ), illustrating transport of the FDOPA tracer into areas of tumor involvement where the blood-brain barrier was still intact. (c) Transaxial T2-weighted images (T2WIs) acquired with a fluid-attenuated inversion recovery (FLAIR) sequence demonstrated abnormal T2 prolongation within the entire area of increased FDOPA uptake ( arrows ), further supporting tumor infiltration into these regions. Tumor invasion into the right temporal lobe ( asterisks ) was also suspected, although without a corresponding focus of FDOPA uptake. This case highlights one of the advantages of PET/magnetic resonance imaging (MRI) relative to MRI alone in the setting of neuro-oncology, as certain tracers can enter the central nervous system to delineate tumor involvement in anatomic regions where the blood-brain barrier remains intact. (Color version of figure available online.)

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Head and Neck Neoplasms

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Figure 4, 64-year-old woman with remote history of facial nerve sparing left parotidectomy for adenoid cystic carcinoma presented with new onset of left facial nerve paralysis. Transaxial T1-weighted images (T1WIs) with 2-deoxy-2-[ 18 F]fluoro-D-glucose-positron emission tomography (FDG-PET) fusion revealed (a) a hypermetabolic mass ( asterisk ) involving the superficial and deep left parotid spaces, (b) increased FDG uptake in the region of the left mental foramen ( arrowhead ), and (d) a focus of FDG avidity at the left mandibular foramen. (c) Transaxial T1WIs demonstrated subtle enlargement of the left mandibular foramen ( arrow ) compared to the contralateral side ( not shown ). These findings were consistent with recurrent malignancy and perineural spread along the expected course of the left inferior alveolar nerve, a diagnosis that likely would have been challenging with PET/computed tomography (CT) or magnetic resonance imaging (MRI) alone. In this regard, PET/MRI can facilitate accurate T staging of head and neck carcinoma. (Color version of figure available online.)

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Thoracic Neoplasms

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Figure 5, 60-year-old woman with a remote history of treated cervical cancer was referred from an outside institution for evaluation of a lung mass. (a) Transaxial contrast-enhanced T1-weighted images (T1WIs) revealed a spiculated right parahilar lung mass ( asterisk ) with mediastinal invasion and near-encasement of the superior vena cava ( arrow ). (b) Transaxial contrast-enhanced T1WIs with 2-deoxy-2-[ 18 F]fluoro-D-glucose-positron emission tomography (FDG-PET) fusion at this same level showed the lesion ( asterisk ) to be hypermetabolic and also identified metastatic lesions of the thoracic spine ( arrowhead ) and left lung hilum ( arrow ). (c) Transaxial contrast-enhanced T1WIs obtained at a more superior level demonstrated lateral extension of the right parahilar lung mass ( asterisk ) with invasion of the chest wall ( arrow ). (d) Transaxial contrast-enhanced T1WIs with FDG-PET fusion at this same level revealed additional sites of metastatic disease in the right ( arrowhead ) and left ( arrow ) aspects of the mediastinum. Subsequent computed tomography (CT)-guided biopsy was positive for squamous cell carcinoma. Given the imaging appearance of the right parahilar mass and the distribution of FDG-avid lymph nodes, these findings were favored to represent metastatic bronchogenic carcinoma rather than recurrence of the patient's treated cervical cancer. These images demonstrate the utility of PET/magnetic resonance imaging (MRI) in detecting and characterizing mediastinal and chest wall invasion by intrathoracic malignancies. (Color version of figure available online.)

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Abdominal Neoplasms

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Figure 6, 70-year-old man with cecal adenocarcinoma status post right hemicolectomy presented for restaging. (a) Transaxial computed tomography (CT) images of the liver revealed small hypodense lesions ( arrows ) that were deemed too small to characterize. Positron emission tomography/magnetic resonance imaging (PET/MRI) was subsequently performed for further evaluation. (b) Transaxial contrast-enhanced T1-weighted images (T1WIs) obtained in the hepatocellular phase of contrast demonstrated two hypoenhancing foci ( arrows ) near the liver dome. (c) Transaxial contrast-enhanced T1WIs with 2-deoxy-2-[ 18 F]fluoro-D-glucose (FDG)-PET fusion showed no definite FDG-avid correlate for these lesions ( arrows ), likely because of their small size and relatively low FDG uptake compared to normal liver. (d) However, diffusion-weighted imaging (DWI) revealed marked diffusion restriction within these lesions ( arrows ) compatible with hypercellular hepatic metastases. This case demonstrates how PET/MRI, when incorporating DWI of the liver, can increase the conspicuity of (and likely also the sensitivity for) hepatic metastases, relative to PET/CT. (Color version of figure available online.)

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Figure 7, 63-year-old woman with history of neuroendocrine tumor arising from the duodenum treated with surgical resection 12 years prior, followed by recurrent oligometastatic disease to the liver status post segment VIII wedge resection 9 months prior, presented for restaging. (a) Transaxial contrast-enhanced T1-weighted images (T1WIs) of the liver revealed numerous arterially enhancing foci throughout the hepatic parenchyma ( arrows ) and at the site of previous segment VIII wedge resection ( arrowhead ). (b) Transaxial T2-weighted images (T2WIs) with DOTANOC-positron emission tomography (PET) fusion demonstrated significant tracer accumulation within the liver parenchyma ( arrows ) and at the site of prior surgical resection ( arrowhead ). DOTANOC binds to somatostatin receptor subtypes 2, 3, and 5, which are expressed by many neuroendocrine tumors (NETs). This case illustrates how the molecular properties of tumors can be exploited by radiotracers to ensure that an abnormality identified on an anatomic image in fact represents the tumor of interest rather than a benign neoplasm or a second unrelated malignancy.

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Pelvic Neoplasms

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Figure 8, 72-year-old woman with a new diagnosis of vaginal small cell carcinoma presented for initial staging. (a) Transaxially-acquired nonisotropic T2-weighted images (T2WIs) showed a tumor ( asterisk ) centered along the anterior aspect of the vaginal canal (v), with extension anteriorly toward the urinary bladder (bl) and posteriorly toward the rectum (r). (b) Sagittal reformat of these nonisotropic T2WIs resulted in a significant degradation of the image quality. Assessment of the relationship between the tumor ( asterisk ) and the adjacent structures was difficult. Transaxially-acquired isotropic T2WIs (c) with 2-deoxy-2-[ 18 F]fluoro-D-glucose-positron emission tomography (FDG-PET) fusion (e) showed invasion of the tumor ( asterisk ) into the posterior urinary bladder wall ( arrow ) and the anterior rectal wall ( arrowhead ). Sagittal reformat of these isotropic T2WIs (d) with FDG-PET fusion (f) much more clearly depicted the full craniocaudal extent of tumor ( asterisk ) invasion into the posterior urinary bladder wall ( arrow ). This case demonstrates the advantages of isotropic magnetic resonance (MR) sequences for the accurate and confident local staging of primary tumors via PET/MRI. (Color version of figure available online.)

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Figure 9, 46-year old woman with newly diagnosed squamous cell carcinoma of the cervix presented for initial staging. Transaxial computed tomography (CT) images (a) with 2-deoxy-2-[ 18 F]fluoro-D-glucose-positron emission tomography (FDG-PET) fusion (c) demonstrated a hypermetabolic soft-tissue nodule ( arrow ) in the region of the right external iliac artery and similar focus of less-intense uptake near the left external iliac artery ( arrowhead ). Differential considerations included nodal metastases, left ovarian metastases, and physiological ovarian uptake. PET/magnetic resonance imaging (MRI) was subsequently performed for further evaluation. Transaxial high-resolution T2-weighted images (T2WIs) (b) with FDG-PET fusion (d) revealed ovoid structures with internal T2-hyperintense cystic spaces compatible with ovaries. There was significant FDG uptake on the right ( arrow ) and trace FDG uptake on the ( left ), similar to the PET findings from the PET/CT examination. Consequently, nodal metastases were excluded from the differential. As with the prior case, the superior soft-tissue contrast of PET/MRI relative to PET/CT also promotes accurate N staging of gynecologic malignancies. (Color version of figure available online.)

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Figure 10, 64-year-old man with an elevated prostate-specific antigen (PSA) level of 7.8 ng/mL presented for imaging evaluation of the prostate gland. Transaxial T2-weighted images (T2WIs) (a) with prostate-specific membrane antigen-positron emission tomography (PSMA-PET) fusion (b) revealed a well-circumscribed hypointense lesion ( asterisk ) with marked PSMA expression. This lesion was located within the right peripheral zone near the apex of the gland. (c) Apparent diffusion coefficient (ADC) map showed a corresponding dark focus ( asterisk ) indicative of restricted diffusion from hypercellular tumor. Relative to magnetic resonance imaging (MRI) only, PET/MRI employing prostate-specific tracers can markedly increase the conspicuity of prostate carcinoma, both within the prostate gland (as this case demonstrates) and elsewhere within the body.

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Figure 11, 50-year-old woman with newly diagnosed rectal adenocarcinoma presented for initial staging. Transaxial isotropic T2-weighted images (T2WIs) (a) with 2-deoxy-2-[ 18 F]fluoro-D-glucose-positron emission tomography (FDG-PET) fusion (b) showed effacement of the fat plane ( long arrow ) between the rectum (r) and the vagina (v) by a large, hypermetabolic tumor arising from the rectum. The fat plane between the urinary bladder (bl) and the vagina was preserved, indicating bladder sparing. Coronal reformats of these isotropic T2WIs (c) with FDG-PET fusion (d) revealed a 10 × 8 mm right internal iliac lymph node ( arrowhead ) that failed to meet size criteria for lymphadenopathy but displayed FDG avidity highly suspicious for nodal metastatic disease. These images demonstrate the ability of PET/magnetic resonance imaging (MRI) to detect tumor spread to lymph nodes that might not appear suspicious on MRI alone because of their normal size and/or morphology, potentially resulting in clinically significant upstaging. (Color version of figure available online.)

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Future Directions

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TABLE 2

Selected Studies Demonstrating Advantages of PET/MRI Over PET/CT

Study Primary Malignancy Findings (PET/MRI Relative to PET/CT)P Value Schaarschmidt et al. Various Fewer indeterminate incidental lesions <0.001 Catalano et al. Various More clinically significant findings <0.001 Beiderwellen et al. Various Higher conspicuity of OMs <0.05 Eiber et al. Various Better anatomic delineation of OMs 0.0001 Kanda et al. Head and neck SCC Superior T staging accuracy 0.041 Grueneisen et al. Breast Superior T staging accuracy <0.05 Donati et al. Various Greater sensitivity for liver metastases 0.002 Nagamachi et al. Pancreatic Better benign vs. malignant differentiation 0.005 Queiroz et al. Gynecologic Superior T staging accuracy <0.001 Kitajima et al. Gynecologic Higher sensitivity for local recurrence 0.041 Park et al. Prostate Better identification of high-grade tumors <0.01

CT, computed tomography; MRI, magnetic resonance imaging; OMs, osseous metastases; PET, positron emission tomography; SCC, squamous cell carcinoma.

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Conclusion

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TABLE 3

Comparison of PET/MRI, PET/CT, and MRI in Oncologic Imaging

Potential advantages of PET/MRI over PET/CT

Potential advantages of PET/MRI over MRI

Potential advantages of PET/CT over PET/MRI

CT, computed tomography; FDG, 2-deoxy-2-[ 18 F]fluoro-D-glucose; MRI, magnetic resonance imaging; PET, positron emission tomography.

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Academic Radiology, Volume 23, Issue 2
Journals General Radiology
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