Abstract
MRI is a very attractive approach for tumour detection and oncological staging with its absence of ionizing radiation, high soft tissue contrast and spatial resolution. Less than 10 years ago the use of Whole Body MRI (WB-MRI) protocols was uncommon due to many limitations, such as the forbidding acquisition times and limited availability. This decade has marked substantial progress in WB-MRI protocols. This very promising technique is rapidly arising from the research world and is becoming a commonly used examination for tumour detection due to recent technological developments and validation of WB-MRI by multiple studies and consensus papers. As a result, WB-MRI is progressively proposed by radiologists as an efficient examination for an expanding range of indications. As the spectrum of its uses becomes wider, radiologists will soon be confronted with the challenges of this technique and be urged to be trained in order to accurately read and report these examinations. The aim of this review is to summarize the validated indications of WB-MRI and present an overview of its most recent advances. This paper will briefly discuss how this examination is performed and which are the recommended sequences along with the future perspectives in the field.
Introduction
For oncological patients, the accurate staging and precise evaluation of the metastatic burden are essential in order to plan an effective treatment. Following treatment, assessment of the change or not in tumour burden is equally essential in order to make decisions related to the continuation or modification of the treatment strategy. Ideally, oncological imaging techniques should be rapid, image a wide part of the body, provide high quality images and clinically significant information. All these requirements bring whole body magnetic resonance Imaging (WB-MRI) to the forefront, as a very attractive technique for tumour detection and response assessment with its lack of ionizing radiation and excellent ability to image both bone marrow and soft tissues. WB-MRI is increasingly used for a wide range of applications thanks to the improved accessibility and technological advances of the last decades.1, 2 The use of diffusion weighted imaging (DWI), transforms WB-MRI to a “hybrid” technique as it provides functional information, enables an “at-a-glance” assessment of the whole body, reduces interpretation time and improves reader’s performance.3–5
Rationale for the use of WB-MRI in oncology
Detection and staging:
In oncology, lesion detection and precise staging are crucial in order to plan an effective treatment and assess prognosis. Many studies have shown that WB-MRI meets these demands thanks to its high performance for tumour detection, its ability to detect bone, node and distant metastasis (Figure 1), as well as the big field of view allowing to image the patient from head-to-toe. Working protocols with set-up in 1.5 and 3 Tesla MRI magnets are summarized in Table 1. In most of the studies, WB-MRI is compared to other staging techniques, such as bone scintigraphy (BS) and positron emission tomography (PET).
Figure 1.

Whole-body MR images in a 75-year-old male with castration-resistant prostate cancer. Coronal T1 weighted MR images (a) and inverted scale DWI images (b-value: 1000 s mm–2) (b) showing a diffuse low signal of the bone marrow on T1 images and a high signal intensity in high b-values DWI (*) indicating diffuse metastatic bone disease, a metastatic lesion of the left lung (arrow) and an abnormal pelvic lymph node (arrow head). Note the discrepancy between T1 and DWI. Homogenous diffuse low signal of the bone marrow on T1 images due to the sclerotic nature of the disease with focal hyper signal lesions on DWI. DWI, diffusion weighted imaging.
Table 1. .
Proposed working protocols with set-up in 1.5 and 3 Tesla magnets
| 1.5 TESLA | ||||
| Sequence | WB 3D T1 WI | SPINE STIR | T2(*) | Whole body DWI | 
| Number of stations × Acquisition time (minutes) | 3 × 3:49 | 3 × 3:32 | 3 × 0.25 | 6 × 2:40 | 
| Sequence type | FSE | FSE | SSH | Diffusion | 
| Plane | Coronal | Sagittal | Axial | Axial | 
| Slices (mm), Thickness (mm), Gap(mm) | 192, 1.4, 0 | 19, 3.5, 0.4 | 44, 4, 0 | 33, 5, 0 | 
| FOV (mm), Acquisition Matrix (mm) | 440 × 440,320 × 320 | 280 × 280, 320 × 256 | 420 × 336, 320 × 224 | 440 × 440, 96 × 128 | 
| Phase encoding | Right/Left | Feet-Head | Anterior-Posterior | Anterior-Posterior | 
| TR (ms), TE (ms) | 400, 12 | 4714, 5 | 562, 8 | 8400, 66 | 
| TI (ms) | / | 140 | / | / | 
| NSA | 1 | 2 | 3 | 1 | 
| Flip angle | varies | 160° | varies | varies | 
| Bandwidth (kHz) | 62.5 | 31.25 | 83.33 | 250 | 
| b-values (s mm–2) | / | / | / | 50, 800 or 0, 1000 | 
| Target gam | Bone, Nodes | Bone (spine) | Liver, Nodes | Bone Nodes, Liver | 
| 3 TESLA | ||||
| Sequence | WB 3D T1 WI | SPINE STIR | T2(*) | Whole body DWI | 
| Number of stations × Acquisition time (minutes) | 4 × 3:59 | 3 × 2:17 | 3 × 0:43 | 4 × 3:36 | 
| Sequence type | 3D TSE | STIR | SSH | Diffusion | 
| Plane | Coronal | Sagittal | Axial | Axial | 
| Slices (mm), Thickness (mm), Gap (mm) | 210, 1.2, 0 | 13, 3.5, 0, 35 | 70, 4, 0 | 50, 6, 0.1 | 
| FOV (mm), Acquisition matrix (mm) | 500 × 300, 440 × 230 | 260 × 260, 260 × 206 | 400 × 300, 308 × 186 | 400 × 352, 100 × 74 | 
| Phase encoding | Feet-Head | Feet-Head | Anterior-Posterior | Anterior-Posterior | 
| TR (ms), TE (ms) | 260, 21 | 3707, 45 | 609, 8 | 6000, 66 | 
| TI | / | 210 | / | / | 
| NSA | 2 | 1 | 1 | 1 | 
| Flip angle | 90° | 130° | 90° | / | 
| Bandwidth (Hz/pixel) | 1052.2 | 565.6 | 629.2× | 107.9 | 
| b-values (s mm–2) | / | / | / | 0, 50, 150, 1000 | 
| Target organ | Bone, Nodes | Bone (spine) | Liver, Nodes | Bone, Nodes,Liver | 
*optional sequence, not routinely used.
Solid tumours
Many studies have underlined the high sensitivity of WB-MRI for the detection of organ metastases, especially for tumours frequently metastasizing to the bone, lymph nodes and liver such as prostate,6–8 breast9, 10 and colorectal cancers.11 There have been reports that WB-MRI can modify a patient’s treatment12 from radical to systemic and vice versa by correctly characterizing a patient as M0 or M1 (Figure 2).
Figure 2.
Whole-body MR images in a 68-year-old female with breast cancer. Bone scintigraphy anterior and posterior views (a), coronal T1 weighted images (b) and inverted scale DWI images (b-value: 1000 s mm–2) (c). The bone scintigraphy is normal, no abnormal foci are observed. WB-MRI study performed 2 days later showing minimum two bone lesions (arrows). Note the last station shading in DWI. DWI, diffusion weighted imaging.
Schmidt et al compared the accuracy of WB-MRI and PET-CT for the staging of various malignant tumours.13 For tumour assessment WB-MRI demonstrated a sensitivity of 86%, for lymph node involvement a sensitivity of 80% and a specificity of 75% and for metastatic disease a sensitivity of 96% and of specificity 82%. In another study by the same team, the diagnostic accuracy of WB-MRI and PET-CT was compared for the detection of tumour recurrence in patients with breast cancer.14 WB-MRI demonstrated an overall diagnostic accuracy of 91% with a sensitivity of 93% and specificity of 86%. PET-CT demonstrated comparable diagnostic accuracy, lower sensitivity (91%) and higher specificity (90%).
A study by Ohno et al showed that in patients with lung cancer, WB-MRI can be used for the M-stage assessment and may be considered at least as effective as fluorine-18 deoxyglucose (18FDG) PET-CT.15 For assessment of head and neck metastases, sensitivity (84.6%), and accuracy (95%) of WB-MRI were significantly higher than those of PET-CT (15.4 and 89.1%, respectively) on a per-site basis. When bone metastases were assessed, specificity (96.1%) and accuracy (94.8%) of WB-MRI were significantly higher than those of PET-CT (88.3 and 88.2%, respectively) on a per-site basis. Interobserver agreements for WB-MRI and PET-CT were similar. The same team recently demonstrated that WB-MRI with DWI is more specific and accurate than 18FDG PET-CT and routine radiological examinations for assessment of recurrence in NSCLC patients.16 WB-MRI with and without DWI demonstrated slightly lower sensitivity.
During the last few years, major developments have been observed in the field of prostate cancer. It has been demonstrated that WB-MRI with DWI is superior to BS with or without targeted X-rays for the detection of bone metastasis.6 In 2014 Shen et al, effectuated a meta-analysis in order to compare the diagnostic performance of Choline PET-CT, MRI, Bone Single Photon Emission CT (SPECT), and BS in detecting bone metastases in patients with prostate cancer.17 Among these modalities, BS demonstrated the lowest sensitivity and specificity when WB-MRI was better than choline PET-CT and BS on a per-patient basis. The pooled specificities for detection of bone metastases using Choline PET-CT, WB-MRI, and BS, were 0.99 [95 % CI (0.93–1.00)], 0.95 [95% CI (0.90–0.97)], and 0.82 [95% CI (0.78–0.85)], respectively. In 2016, Conde-Moreno et al compared 18F-Fluorocholine PET-CT and WB-MRI with DWI for the detection of bone and/or lymph node metastases in oligometastatic prostate cancer patients.18 The authors concluded that WB-MRI and Choline PET–CT are complementary techniques. 35 patients were analysed and when comparing the standard work-up (BS, CT and pelvic MRI) with the combination of WB-MRI and Choline PET-CT, 16 patients went from being non-metastatic to metastatic (45.7%), five from being oligometastatic to polymetastatic (14.2%) and finally two went from being considered metastatic to M0 (5.7%). Only 12 remained at the same staging (34.3%). On the contrary, a recent study compared 11C-Choline PET-CT and WB-MRI including DWI for patients with recurrent prostate cancer and found that PET-CT is superior for the detection of local recurrence and bone metastasis on a regional basis when WB-MRI showed similar diagnostic accuracy only for detecting LN metastases.19 The authors concluded that WB-MRI cannot serve as an alternative imaging modality for restaging prostate cancer.
A relatively new technique for prostate cancer detection is the Prostate Specific Membrane Antigen (PSMA) PET-CT. PSMA is a cell surface protein overexpressed by prostate cancer cells. Ligands of PSMA are labeled with 68Ga,99mTc and123/124/131I for the detection of Prostate cancer metastases or relapse20–22 (Figure 3). Gupta et al compared the diagnostic accuracy of 68Ga PSMA PET-CT and MRI of the pelvis for the detection of LN metastasis in patients with high risk prostate cancer.23 PET-CT was superior for the detection of pathological lymph nodes with diagnostic sensitivity, specificity, positive predicative value (PPV), negative predicative value (NPV), and accuracy 100, 80, 87.5, 100, 91.67%, vs 57.14, 80, 80, 57.4, 66.67%, respectively for the MRI. In 2015, Afshar-Oromieh et al studied the diagnostic value of PET-CT imaging with the new 68Ga-labelled PSMA ligand HBED-CC (68Ga-DKFZ-PSMA-11) for the diagnosis of prostate cancer.24 The authors showed that PET-CT can detect prostate cancer in a high percentage of patients with suspected cancer (82.8%) and the tracer is highly specific for this tumour. The lesion-based analysis of sensitivity, specificity, NPV and PPV revealed values of 76.6, 100, 91.4 and 100%. Obek et al demonstrated that 68Ga PSMA PET-CT is superior to morphological imaging for the detection of metastatic LN in patients with primary prostate cancer, even though surgical dissection remains the gold standard for precise lymphatic staging.25
Figure 3.
68Ga-PSMA PET CT (a) and WB-MRI (b, c, d) in a 82-year-old patient with high risk for metastasis prostate cancer (a): Clearly visible pathological accumulation of the radiotracer at the level of the spine (arrows) indicating metastatic bone disease and at the level of the pelvis (arrow head) demonstrating the presence of an abnormal lymph node (b–d): Coronal T1 weighted MR images (b, c) and inverted scale DWI images (d, b-value: 1000 s mm–2) (c) with the same findings. Multiple bone marrow metastasis at the level of the spine (arrows) and an abnormal pelvic lymph node (arrow head). Note the splenomegaly as the patient suffers from mild liver failure. DWI, diffusion weighted imaging; PET, positron emission tomography.
Even though there is evidence that choline PET-CT and WB-MRI are superior than BS for the detection of metastatic bone disease in PCa, the clinical benefit of detecting bone disease at an earlier time point remains to be studied further. Therefore, according to the European Association of Urology (EAU) guidelines, for high risk PCa patients, the metastatic staging should include at least a cross sectional abdomino-pelvic imaging and BS.26
In the field of testicular cancer WB-MRI is very promising due to the usually young age of the patients and the surveillance protocol which in some cases demands frequent imaging by CT27, 28 (Figure 4). Mosavi et al evaluated the feasibility of WB-MRI with DWI for the follow up of these patients.29 The authors demonstrated that WB-MRI is feasible and DWI offers functional information concerning the residual masses. Sohaib et al investigated the sensitivity of WB-MRI for the detection of retroperitoneal lymph nodes in patients with germ cells tumours.30 The authors compared the retroperitoneal node detection of WB-MRI to CT and concluded that MRI has comparable sensitivity and is not inferior to CT which is the standard imaging technique at the time being. It has to be noted that DWI was not used in the WB-MRI protocol.
Figure 4.

Whole-body MR images in a 25-year-old male with testicular seminoma. Coronal T1 weighted MR images (a) and and inverted scale DWI images (b-value: 1000 s mm–2) (b) show a pathologic retroperitoneal lymph node (arrow). DWI, diffusion weighted imaging.
Neuroendocrine tumours (NET) are a heterogeneous family of slow-growing malignancies arising from the neuroendocrine cells. Most NET cells express somatostatin receptors (SSR), which can be targeted by labelled somatostatin analogues. There are many studies demonstrating that PET-CT in combination with 68Ga-labelled SSA is very useful for the diagnosis of NETs.31–33 Carlbom et al compared the use of WB-MRI with DWI and liver-specific contrast agent-enhanced imaging to (11C)−5-Hydroxytryptophan PET-CT (5-HTP PET-CT) for the detection of NETs.34 17 of 28 patients (61%) showed complete concordance between WB-MRI and the PET-CT examinations. There were three patients with lesions that were detected by PET-CT but not by MRI, four patients with liver lesions that were detected by MRI but not by PET-CT, and three patients with MRI-only detected lesions in other locations (1 or 2 lesions per patient). The authors concluded WB-MRI with contrast enhanced liver sequences is superior for the detection of liver metastases but did not detect all NET lesions spotted with 5-HTP PET-CT. In a prospective study Etchebehere et al compared 99mTc-hydrazinonicotinamide (HYNIC)-octreotide SPECT-CT, 68Ga-DOTATATE PET-CT, and WB-MRI with DWI for the detection of NET lesions.35 The authors demonstrated that 68Ga PET-CT appears to be more sensitive for detection of well-differentiated NET lesions, especially for bone and unknown primary lesions. Moryoussef et al showed that the addition of DWI in the WB-MRI protocol revealed additional findings in 71.4% of the patients compared to WB-MRI alone, with 72.4% more lesions, mainly infracentimetric.36 These observations lead to the modification of the therapeutic management for 19% of the patients.
Melanoma
In a prospective study, Muller-Horvat et al compared the efficacy of WB-MRI with conventional Whole Body CT (WB-CT) in 43 patients with advanced malignant melanoma and demonstrated that WB-MRI was more sensitive than the standard imaging for the detection of solid metastases.37 WB-CT was more sensitive for the detection of lung metastases, even though WB-MRI correctly identified all lung nodules larger than 5 mm. One year later, Pfannenberg et al compared the overall and site-based accuracy of 18FDG PET-CT and WB-MRI. The overall accuracy in the lesion-based evaluation was 86.7% for PET-CT, 78.8% for WB-MRI, 75.0% for CT and 74.3% for PET alone.38 The differences between PET-CT and WB-MRI, as well as between PET-CT and PET alone were significant. In 2010, Laurent et al compared WB-MRI with a multicontrast protocol and DWI to 18FDG PET-CT.39 For the overall accuracy evaluation, the sensitivity was 88.6% for WB-MRI and 72.9% for PET-CT and the specificity was 97.6% for WB-MRI and 92.7% for PET-CT. MRI was the best modality for staging liver metastases, as PET-CT failed to identify two metastases. Regarding bone and skeletal metastases, MRI was also superior. Petralia et al studied 19 patients in order to investigate whether WB-DWI alone is adequate for detecting metastases in melanoma patients or if WB contrast-enhanced MRI is required.40 They concluded that WB-DWI is promising for the detection of extracranial metastases (lung metastases greater than 5 mm and even smaller metastases in the abdomen, pelvis, bones, and subcutaneous tissues) but contrast enhanced MRI is required for the evaluation of the metastatic brain disease. The German evidence based guideline for cutaneous melanoma recommend the use of PET-CT for detection of extra-cranial metastatic disease even though it is specified that whole body MRI may also be used as alternative.41 The Swiss guidelines recommend the use of CT, MRI, PET or PET-CT every 1–5 years for the follow up of patients with Stage IIC, III et IV tumours.42
Haematological cancers
WB-MRI is a very useful tool for the imaging of patients with monoclonal plasma cell disease (Figure 5). MRI has the highest sensitivity for detecting bone marrow involvement.43, 44 The recent consensus statement from the International Myeloma Working Group (IMWG) has recommended WB-MRI for the work-up of solitary bone plasmacytoma and all patients suspected of having asymptomatic or smoldering multiple myeloma (MM).45 According to the authors, MRI provides significant prognostic information in patients with symptomatic disease and may be found useful in the better definition of complete remission. Furthermore the National Institute for Health and Care Excellence (NICE) guidelines for myeloma state that WB-MRI should be used as first line examination before WB-CT and X-rays.46 Chantry et al also recommend the use of WB-MRI in patients with MM pointing out that this technique has prognostic value and should be used in the assessment of treatment response.47 Bäuerle et al demonstrated that WB-MRI should be preferred over spine MRI for patients with a MM or monoclonal gammopathy of undetermined significance (MGUS).48 In their study the authors showed that the lesions were confined to the spine or sacral bone in only 11 out of 48 patients with bone involvement. In nine patients, the lesions were located only outside the spine, and in 28 patients the lesions were found both axially and extra-axially. The authors concluded that the detection of nearly 50% of the patients with monoclonal plasma cell would have been missed by spine MR imaging.
Figure 5.
Whole-body MR images in a 68-year-old male with multiple myeloma. Coronal STIR (Short tau inversion recovery) (a) and T1 weighted (b) MR images and inverted scale DWI images (b-value: 1000 s mm–2) (c). The bone marrow shows diffuse hyperintense signal in STIR (a,*), hypointense signal in T1 (b, *) and high signal intensity in high b-value DWI (c,*) indicating diffuse tumoral infiltration (spine, pelvis, femora, humeri and ribs). Two dorsal vertebral fractures are observed (arrows). X-ray of the skull (d) demonstrating multiple lytic lesions (arrows).
In a recent study Rasche et al investigated newly diagnosed MM patients using simultaneous FDG-PET and WB-DWI, in order to describe the proportion of PET false-negative patients and to identify tumour-intrinsic features associated with PET false-negativity.49 In 11% of patients, WB-DWI was positive (DWI+) for disease when no apparent disease involvement was detected using PET-CT (PET–). In order to shed light on this “PET false-negativity” phenomenon, the authors compared the gene expression profiling data derived from the DWI + /PET + and DWI + /PET cases. The results showed a strong association between low hexokinase-2 expression and false negative FDG-PET examination results. In respect to these results, WB-DWI is arising as a very efficient alternative examination in these patients.
Dixon imaging is an approach for fat suppression using simple spectroscopic imaging, published by Dixon in 1984.50 With this technique two different images are obtained: a conventional image with water and fat signals in phase (IP) and a second one so that fat and water signals are 180° out of phase (OP). From these two images a water only (WO) and a fat only (FO) images are acquired. The water only sequence is very useful thanks to the fat suppression. Bray et al studied the diagnostic utility of WB Dixon MRI in MM.51 30 patients with clinically-suspected MM underwent WB-MRI and unenhanced Dixon IP, OP, WO and FO images were obtained and analysed. The authors demonstrated that FO images were superior to the other concerning lesion counts, true positives, sensitivity and confidence. Additionally, the contrast to noise ratio was higher for FO than IP images. Also, the FO sequence offered the greatest advantage for patients with focal lesions, but also provided superior sensitivity in patients with diffuse disease. The authors conclude that in order to improve diagnostic efficacy and reporting, the radiologists should preferably review FO images.
The diagnosis of bone marrow involvement in lymphoma is of great importance because its presence indicates the highest Ann Arbor stage (Stage IV) and may have therapeutic and prognostic implications.52, 53 Blind bone marrow biopsy (BMB), usually of the posterior iliac crest-even though it is an invasive and painful procedure prone to sampling errors and false-negatives remains the standard diagnostic test for the assessment of the bone marrow in lymphoma.54–57
WB-MRI has emerged as a very promising technique for nodal and extranodal staging of lymphoma.58–60 Recently Albano et al compared WB-MRI with DWI, 18FDG PET-CT and BMB, for the evaluation of bone marrow involvement in patients with newly diagnosed lymphoma.60 According to the authors, both WB-MRI and PET-CT showed very high reliability in the detection of bone marrow involvement. The two techniques were concordant in all cases of diffuse large B-cell and follicular lymphomas but had low sensitivity for the detection of low volume bone marrow involvement in mantle cell and marginal zone lymphomas. A more recent study by Adams et al assessed the prognostic implications of WB-MRI findings in diffuse large B-cell lymphoma patients with a negative blind BMB and demonstrated that WB-MRI has prognostic implications in these patients as it can modify their Ann Harbor score.59 The authors concluded that disease relapse or progression and death occur more frequently in WB-MRI positive patients than in WB-MRI negative patients. An older study by Tsunoda et al demonstrated that abnormal MRI signal of the patients’ femoral bone marrow, is associated with a significantly poorer survival, regardless of histologic findings of the BMB.61
Whole body MRI can play an important role in the imaging of lymphomas with poor 18FDG avidity as low grade lymphomas. Although most lymphoma subtypes have been shown to be highly avid to 18FDG, there are some subtypes with lower avidity such as small cell lymphocytic lymphoma,62, 63 peripheral T-cell lymphoma64 and extranodal marginal zone lymphomas, including the mucosa-associated lymphoid tissue (MALT) marginal zone lymphoma.63 Last but not least, utility of whole-body MRI as a radiation-free alternative to FDG-PET-CT for staging of pregnant patients with malignant lymphoma has to be highlighted. It has to be underlined that the use of gadolinium should be limited only in cases which the benefits clearly outweigh the possible risks for the fetus.65
WB-MRI as screening tool
WB-MRI can be used as a tool for cancer screening in patients with genetic predisposition to develop tumours.66–68 It is common knowledge that the outcome of the oncological patients improves when the tumour is identified at earlier stages. Some of the syndromes that are mentioned in the literature are multiple endocrine neoplasias I and II (such as endocrine tumours), Von Hippel-Lindau syndrome (such as renal carcinomas), familial adenomatous polyposis (such as colorectal tumours), and Li-Fraumeni syndrome (various types of tumours including sarcomas).
Quite recently Anupindi et al proposed the use of a WB-MRI protocol for the screening of children with cancer-predisposing conditions.69 The WB-MRI protocol consisted of multiple anatomic sequences, without the use of intravenous contrast. WB-DWI was not consistently used in this study.
A recent meta-analysis by Ballinger et al investigated whether WB-MRI can detect asymptomatic cancers in a curable stage in patients with Li-Fraumeni syndrome, carriers of TP53 gene.70 Baseline WBMRI identified a new and treatable malignant neoplasm in 7% of the patients. The authors concluded that WB-MRI is a useful tool for early detection of neoplasms in this cancer-prone population and its use could be proposed for the routine baseline assessment of TP53 mutation carriers.
WB-MRI can be used in multiple tumours disease such as Langerhans cell histiocytosis and hereditary multiple exostoses syndrome in order to evaluate the disease.71 Hardes et al suggested the use of WB-MRI in cases of multifocal vascular tumours as angiosarcoma.72 Jasperson et al evaluated the value of WB-MRI as a screening method in families with succinate dehydrogenase (SDH)-associated hereditary paragangliomas and recommended the use of this modality combined with traditional biochemical testing.73
Whole body MRI: how to do it?
General considerations
There are several technical challenges to overcome, in order to perform WB-MRI. First, the acquisition of good quality images necessitates the main magnetic field to be strong enough in order to provide a high signal to noise ratio (SNR); as a result, using a minimum of a 1.5 Tesla magnet is a prerequisite.74 3.0 Tesla magnets provide higher SNR for anatomic sequences. On the other hand DWI sequences are less robust when acquired with 3.0 Tesla than 1.5 Tesla magnets because the sequence is more prone to artefacts.74
Second, WB-MRI coverage requires the development of multistation techniques in which the different body regions are scanned step by step and the individual data are combined and composed in order to acquire a WB image. In recent years, the development and use of a high-performance gradient and radiofrequency systems provide rapid image acquisition and homogenous excitation of large volumes retrospectively. Thanks to these technological advances, the acquisition time can be reduced without significantly sacrificing the quality of the images.50, 51 Moreover, three dimensional (3D) acquisition images can be acquired as well as anatomical imaging with different weighting (water, fat).50, 51
Thirdly, the inclusion of a WB-DWI into a WB-MRI protocol increases the diagnostic performance of the protocol in various cancers.1, 75 WB-DWI does not require breath-holding or respiratory triggering and as a result the scanning time is no longer a limiting factor. Thin slices are acquired with the possibility of 3D reconstructions as maximum intensity projections (MIPs), volume rendering, and multiplanar reformatting (MPR). Images with different diffusion weighting (i.e. with different b-values) can be acquired with the additional possibility to calculate an intra-lesional Apparent Diffusion Coefficient (ADC), or to reconstruct an ADC map of the region of interest; these latest approaches improve the detection of lesions and allow quantitative characterization.
Fourth, advanced image post-processing is required for the quantitative analysis of response to treatment. Accurate co-registration (i.e. accurate spatial alignment) of different examinations or of different imaging modalities have to be achieved first.
Which sequence and which plane?
A review of the literature reveals that depending on the team and acquisition time, WB-MRI protocols consist of only anatomic or anatomic and functional (DWI) sequences.75 While the interest of WB-DWI within a WB protocol is not contested (even if further work is needed to understand how to implement it optimally), an important heterogeneity is observed between different countries, centres and teams regarding the anatomic sequences and acquisition planes.
Some teams use T1 and STIR sequences of the whole body in coronal76–79 or axial plane, others only one of these anatomic sequences.7,9,80–83
Recent studies have demonstrated the utility of WB Dixon imaging.51,84–88 Thus, Dixon sequences are increasing in popularity for the detection of bone lesions in oncological patients, as they offer high quality images in shorter acquisition time than classic spin echo images. Bone marrow fat fraction maps have to be generated, when Dixon images are obtained.89–91 In order to calculate fat fractions from gradient-echo Dixon scans, the acquired images should be proton density weighted. Depending on the sequence parameters (flip angle, repetition time), some residual T1 weighting may result. In this case, the estimated fat fractions become inaccurate, but can be corrected by using literature values for the T1 of fat and the tissue of interest.
Furthermore, Dixon sequences offer good fat suppression images in obese patients.92 The conspicuity of bone metastasis with each of the Dixon sequences was studied by Costello et al in 2013.88 The authors concluded that in fast Dixon WB-MRI protocols, FS T1 with contrast sagittal, FO T1 with contrast sagittal, T1 with Contrast sagittal, and FS T1 with contrast axial sequences had significantly higher conspicuity for bone metastases compared to other sequences.
Regarding the acquisition plane, the coronal is widely used because it enables fast coverage of larger parts of the body, even though there are some limitations concerning the visualization of the long bones, skull, sternum, scapula and ribs. A dedicated plane can be added in order to better visualize certain structures, as a whole spine sagittal plane or an axial plane for the visualization of the ribcage and the sternum.6, 7,81,93,94
A new 3D T1 WB-MRI (WB 3D T1) anatomic sequence has been developed that could potentially replace the different anatomic components of WB-MRI protocols for the bone and node staging of cancer patients.95 This new sequence can be reconstructed in any plane, is of millimetric resolution and demonstrates enhanced image quality, compared to the two-dimensional (2D) sequences utilized until now (Figure 6).
Figure 6.
Whole-body 3D MR images in a 70-year-old male with prostate cancer (a) Coronal reconstructed image showing bone marrow metastasis of right iliac bone (arrows) and an abnormal iliac lymph node (arrow head) (b) Sagittal reconstructed image showing multiple bone marrow metastasis of the spine (arrows) (c1 and c2). Axial reconstructed images showing bone marrow metastasis of a left rib (arrows in c1) and an abnormal para-aortic lymph node (arrow in c2).
Currently there is an urgent need for standardization and better evaluation of the clinical benefit of WB-MRI protocols. There are no clear recommendations stating which sequences should be used and in which plane, apart from prostate cancer. Padhani et al in METastasis Reporting and Data System for prostate cancer (MET-RADS), recommend the use of WB-DWI in axial plane (minimum 2 b-values), and for the anatomic counterpart T1 and STIR sagittal sequences of the spine, a WB T1 gradient echo (GRE) Dixon sequence in axial or coronal plane (or both) and optionally a WB T2 W TSE without fat-suppression in axial plane.96
However, according to Ohlmann-Knafo et al WB-MRI protocols for bone metastases detection could safely be limited to the T1 sequence especially at 3 Tesla magnets.97 According to the authors the STIR sequence can be omitted as it does not offer better performance nor modifies the diagnosis made by T1 sequences alone.
Latest developments of whole body MRI in oncology
Treatment monitoring and prognosis
Even though WB-MRI protocols have been shown to be promising in the evaluation of treatment2,90,96,98–100 the radiological community is still busy searching for pertinent and robust (i.e. clinically validated) imaging biomarkers for the follow up of oncological patients (Figures 7 and 8). WB protocols with DWI sequences along with anatomical imaging can potentially generate these markers. The pertinence of parameters such as the (total) tumour volume, the ADC (or measurements derived from the ADC such as the total diffusion volume, the functional response map or the ADC histograms), or the signal fat fraction are currently under investigation.
Figure 7.
Progressive disease in a patient on androgen deprivation therapy whole body MRI images in a 69-year-old patient with prostate cancer. (a–d): Baseline examination and (e–h): 6 months follow up (a–c, e–g): Coronal T1 weighted MR images (d, h): Reconstructed maximal intensity projection image from inverted scale DWI images (b-value: 1000 s mm–2) (a–d): Sternal (arrows) and dorsal spine (arrow heads) bone marrow metastasis and a normal sized left iliac lymph node (dotted arrow) (e–h): increase in size (e–g) and in high b-value signal intensity (h) of sternal (arrows) and dorsal spine (arrow heads) bone marrow lesions and increase in size of the abnormal lymph node.
Figure 8.
Response to treatment in a patient on androgen deprivation therapy Whole body MRI images in 50-year-old patient with prostate cancer. (a–c): Baseline examination, (d–f): 6 months follow up, (h, i): 1 year follow-up (a, b, d, e, h, i): Coronal T1 weighted MR images (f): dorsal region of (e), magnified (b, g, j): Reconstructed maximal intensity projection image from inverted scale DWI images (b-value: 1000 s mm–2) (a–c): Multiple bone marrow metastasis (arrows) and abnormal pelvic lymph nodes (arrow heads) (d–i): Decrease in size and in signal intensity in T1 sequence (d, e, h, i) of the spine (arrows) and left femoral (dotted arrows). Emergence of peritumoral hyperintense fat around the dorsal lesions (f-arrow) and decrease in signal intensity in T1 sequences (d, e, h, i). Decrease in signal intensity in high b-values DWI for the dorsal lesions (g- arrows) and disappearance of the left femoral lesion (g-dotted arrow). Decrease in size (d, e, h) of the pelvic lymph nodes (arrow heads). DWI, diffusion weighted imaging.
In patients with MM, Horger et al observed that DWI measurements accurately correlated with the course of the disease, according to clinical and laboratory criteria.98 Messiou et al demonstrated that marrow ADC values (derived from MRI of the spine and pelvis) in patients with active myeloma are significantly higher than in patients in remission.90 ADC increased at 4–6 weeks and decreased at 20 weeks in responders. In progressing and stable patients, ADC did not change significantly between time points. In 2012 Mertz et al studied the prognostic significance of longitudinally performed WB-MRI in patients with smoldering myeloma.101 WB-MRI contributed to the risk stratification in these patients and defined a group that had high risk of progression to MM. The authors analysed 63 patients with smoldering myeloma which had at least two WB-MRIs for follow-up. Progressive disease in the second WB-MRI was of prognostic significance.
Bannas et al compared the diagnostic performance of WB-MRI with haematological parameters (monoclonal protein concentration, serum protein electrophoresis, monoclonal immunoglobulin, immunofixation electrophoresis) for detecting persistent or relapsing disease in patients with MM after stem cell transplantation.102 The authors concluded that even though WB-he is very convenient and well suited for the localization of intra- and extramedullary disease, it demonstrated only moderate agreement between with serum analyses when assessing response to therapy
In 2015, Takasu et al demonstrated that fat signal fraction derived from Dixon sequence can be used as a biomarker in order to discriminate symptomatic from asymptomatic myeloma.91 The authors proved that fat signal fraction offers superior sensitivity and specificity to bone marrow plasma cell percent of biopsy specimens.
Latifoltojar et al proved that patients with MM who demonstrate response to treatment, show a significant increase in signal fat fraction, compared to no significant change in non-responders.89 At 8 weeks, a reduction in estimated tumour volume (eTV) was observed, as well as an increase in signal fat fraction and ADC in the group as a whole. Patients with complete/very good partial response had a significantly greater increase in signal fat fraction compared to those achieving partial response. The same team studied 21 patients with MM who underwent WB-MRI with DWI sequences at diagnosis and after two cycles of chemotherapy. ADC increased significantly following treatment in 7/14 responders.84 After treatment in the non-responders group, ADC did not change significantly in 4/6 patients, and increased in 2/6. The authors concluded that the ADC significantly increased in responders but not in the non-responders.
Mayerhoefer et al studied whether interim 18FDG PET-CT or WB-DWI can predict the end of treatment outcome after immunotherapy in patients with MALT.103 Patients with untreated MALT lymphoma prospectively underwent 18FDG PET-CT and WB-DWI before treatment and after three cycles of rituximab-based immunotherapy. Maximum and mean standardized uptake values (SUVmax and SUVmean respectively), and minimum and mean apparent diffusion coefficients (ADCmin and ADCmean respectively), were measured for up to three target lesions per patient. The authors also measured the rates of change between baseline and interim examinations (ΔSUVmax, ΔSUVmean, ΔADCmin, and ΔADCmean). The authors found significant differences between complete remission and partial remission for parameters ΔSUVmax, ΔSUVmean, and ΔADCmin and between complete remission and stable disease for parameters ΔSUVmax, ΔSUVmean, ΔADCmin and ΔADCmean.
WB-DWI can be used as an indicator of response to treatment, since the data from the sequence can be quantified and used in order to construct parametric maps. In a pilot study, Blackledge et al performed a small cohort of patients with bone metastases who were classified as non-responders to treatment. They observed a significantly larger percentage increase in their total Diffusion Volume (tDV) after treatment, compared to responders.104 Among the responders, there was a significant decrease in tDV, an increase in the median global Apparent Diffusion Coefficient (gADC) and gADC variance.
Perez-Lopez et al proved that WB-DWI can be used for the assessment of metastatic bone disease in patients with prostate cancer.105 The authors demonstrated that there is a strong correlation between tDV and overall survival of these patients. A year later, the same team indicated that patients which show response to olaparib present a decrease in tDV and an increase in median ADC of bone metastases.106
Concerning metastatic bone disease in patients with prostate cancer, Messiou et al studied 26 patients with bone metastases who underwent DWI MRI of the lumbar spine and pelvis at baseline and 12 weeks following chemotherapy.107 The authors indicated that ADC and true diffusion ADC without contribution of perfusion, increase significantly in lesions of both responders and progressors and concluded that mean ADC is not an appropriate biomarker for disease response. In contrast to these results, Reischauer et al demonstrated that DWI MRI allows monitoring of hormonotherapy in patients with prostate cancer and bone metastases.108 Mean tumour ADC increased in response to hormonotherapy and corresponded well with a decrease in PSA.
Padhani et al proposed the MET-RADS imaging recommendations for tumour detection and treatment evaluation in patients with advanced prostate cancer.96 The main aims of this reporting system are to develop complete and detailed response criteria for bone, soft tissue and local disease assessment, in order to establish the minimum acceptable technical requirements for WB-MRI and to educate the radiologists with an aim to reduce the variability in interpretations.
Recently Kosmin et al investigated whether there is any additional benefit in using WB-MRI alongside restaging thoraco-abdominal CT scans in patients with metastatic breast cancer.12 The authors showed that WB-MRI detected additional sites of disease not reported by the CT, mostly in bone. Moreover, in 46 cases (28%) there were differences concerning the response to treatment between WB-MRI and CT. From these cases 89.1% showed evidence of either disease progression or partial response that was reported as stable disease on CT. The systemic anti-cancer therapy was significantly modified following the additional information provided by that WB-MRI, but it is unclear whether this improved the patient outcome.
WB-MRI and oligometastatic patients
Solid tumours that have given distant metastasis are considered incurable with few exceptions such as germ cell tumours and colon cancer. Lately, the subject of oligometastatic patients is receiving more and more attention by the scientific community. In 1995, Hellman and Weichselbaum introduced the term of “oligometastases”.109 The authors suggested that there are intermediate tumour states between purely localized cancer and metastatic and that the oligometastatic patients could be good candidates for curative treatment. For patients with breast cancer, the existing guidelines recommend surgery, radiation, and regional chemotherapy as possible therapeutic options in patients with localized metastatic disease.110 According to the consensus recommendations of The European School of Oncology–Metastatic Breast Cancer (ESO–MBC) “A small but very important subset of metastatic breast cancer patients, for example those with a solitary metastatic lesion, can achieve complete remission and a long survival. A more aggressive and multidisciplinary approach should be considered for these selected patients”.111
Even though according to St. Gallen Advanced Prostate Cancer Consensus Conference (APCCC) 2015, prostate cancer patients with 3 or less synchronous metastases (bone and/or lymph nodes) were considered to be oligometastatic,112 the new APCCC 2017 panel did not reach a consensus.113 10% of the panelists did not believe that “oligometastatic prostate cancer” is a clinically meaningful entity. From the panelists that believed in the definition of “oligometastatic” patients, 14% voted for ≤2 metastases, 66% for ≤3 metastases, and 20% voted for ≤5 metastases as a cut-off for the number of metastases to consider a patient as “oligometastatic”.
There is now a significant amount of studies suggesting that there is a survival benefit if these males have radical treatment of their primary tumour alongside “metastasis-directed therapy”.114 A recent meta-analysis concluded that metastasis-directed therapy with surgery and/or radiotherapy instead of a systematic approach, is very promising although the low level of evidence does not allow its recommendation as standard of care.114 Undoubtedly for these treatment options to be successful, the accurate and proper characterization of a patient as “oligometastatic” and the correct identification of all the metastatic sites are crucial.
The important role of new imaging techniques that are capable of accurately detecting metastatic lesions as WB-MRI with DWI and PET-CT is highlighted by various recent studies.112, 115 New robust techniques such as PET-CT and WB-MRI with DWI have the greatest versatility in terms of metastasis detection even though current guidelines and recommendations remain based on conventional imaging modalities.112, 115 In a recent study, Larbi et al demonstrated that the proportion of prostate cancer patients with oligometastatic disease can be accurately determined by WB-MRI + DWI.116 This study also provided a “map” demonstrating the distribution of lymph node metastases.
“All in one” WB-MRI protocols
The multimodality algorithms that are used for the TNM staging of cancer patients necessitate multiple hospital visits and appointments in different departments (Radiology and Nuclear Medicine departments), leading inevitably to additional waiting times and discomfort for this fragile group of patients (elderly with multiple comorbidities). In order to save time, single modality protocols have been developed and are used in clinical practice.
In 2003 Antoch et al emphasized on the potential of single examinations for the staging of oncological patients.117 The team studied the performance of WB-MRI and FDG PET-CT for the overall TNM classification of 98 patients with various malignant tumours and concluded that PET-CT was significantly superior to WB MRI.
The use of WB-MRI protocols can allow the complete disease assessment in one single examination including detection of metastasis sites which reduces the number of hospital visits for the patients.7, 118 In 2013, anatomic and functional WB-MRI sequences were combined with a multiparametric MRI (mpMRI) of the prostate, in order to obtain the complete TNM staging of prostate patients in a single step MRI protocol7 (Figure 9). This new “one step” protocol outperforms the current techniques (thoraco-abdominal CT for N staging and Bone Scintigraphy with X-rays when necessary for M staging) for the staging of newly diagnosed patients. In accordance with these results, the team of Robertson et al confirmed these results and demonstrated that WB-MRI with a dedicated prostate MRI is feasible in clinical routine and provides clinically important information in patients with suspected recurrent prostate cancer.119 The MET-RADS imaging recommendations were also formulated in order to study all manifestations of advanced prostate cancer in one WB-MRI examination.96
Figure 9.
“All in one” WB-MRI protocol for the TNM staging of a high risk for metastasis in a 74-year-old prostate cancer patient. One single step protocol combining a multiparametric MRI of the prostate (a, b) for the T and a WB-MRI protocol (c– f) for the N and M staging. T2 axial images (a) and ADC map (b) of the prostate demonstrating a low signal intensity mass with low ADC values (arrows). No capsular invasion. Coronal T1 weighted WB-MRI images (c, d) and inverted scale DWI images (b-value: 1000 s mm–2) (e, f) showing a metastatic bone marrow lesion of the right ischio-pubic ramous (arrows) and abnormal retro-peritoneal and pelvic lymph nodes (arrow heads). The TNM staging of this patient is T2N1M1.
Problems to be solved and future perspectives
Cost and examination time
The two major obstacles in making the use of WB-MRI more widespread are elevated cost and longer scan times. While the MR examination time is a general concern, it becomes of paramount importance for oncologic patients who may be frail and/or in pain. WB-MRI protocols have to be constructed to include only the necessary, but sufficient sequences to answer the clinical question.
There have been many innovations in order to overcome the limit of time during the last years120–122 but there is still a lot of work in progress. Possible strategies for the acceleration of data acquisition are the use of standard techniques (minimizing the number of signal averages, reduced scan percentage), half scan (half Fourier imaging), rectangular FOV), parallel imaging techniques (SENSE, GRAPPA etc) and the use of sparse MRI (compressed sensing). In order to reduce the acquisition time, for the anatomic sequences the plane that is usually implemented is the coronal and for the DWI, only two b-values can be used in staging. Furthermore, scan time of “All in one” WB-MRI will most probably decrease in the future as new studies support that for prostate MRI, abbreviated biparametric protocols demonstrate equivalent performance to multiparametric ones.123, 124 A decrease in acquisition time will mean a reduction in cost and an increase in MRI machine availability, as both of these factors are dictated by scan duration. Less time spent on the machine will also mean higher level of patient comfort and reduction of movement artefacts.
Standardization of WB-MRI protocols
It is widely acceptable that there is an immediate need for standardization and uniformity of WB-MRI protocols before the literature becomes as frustrating and puzzling as a “tower of Babel”, as it was suggested by Turkbey and Choyke.125 The uniformity and standardization of WB-MRI protocols will promote a better communication between imaging specialists and clinicians and will encourage the quality assurance.
A big step forward towards this direction was recently made by Padhani et al.96 The team described the recommendations to standardize the WB-MRI protocols for the imaging of patients with advanced prostate cancer.96 The authors stated the minimum acceptable technical requirements and proposed a complete WB-MRI protocol including functional and anatomical sequences. For every examination, the radiologist should complete a structured clinical and radiological template. This report should contain the indication, details of the technique, the findings with description and measurements of the lesions and finally a clear and brief conclusion summing up the overall assessment of the disease status.
Of course, in order to make WB-MRI an effective examination for cancer detection and staging, radiologists have to be educated and given the skills to implement and interpret WB-MRI images. Insufficiently educated radiologists will not be able to keep up with the rising demands of clinicians and this creates a vicious cycle. They have to be coached on the right indications, what the clinician needs to know and expects from them, how to interpret the images and draw conclusions concerning response or not to treatment. Detailed practice guideline statements and properly updated training courses are necessary steps to reach this objective.
Post-processing of WB-MRI data
To date, there is a critical lack of imaging tools to ease the analysis of WB-MRI data. Very few options exist to help in lesion detection, track the same lesion in consecutive follow-ups, and finally demonstrate automatically the evolution of functional parameters (like the ADC) during the disease.
Intensity standardization between stations and then co-registration algorithms are needed to spatially re-align the multiple stations acquired and to obtain an exact anatomical match between anatomical and functional data.
New technologies are being developed to accurately compare successive examinations with each other. Various strategies are currently investigated for research purposes126–128 and the development of tools for segmentation and lesion detection remains a focus of ongoing research.
For image processing and disease segmentation, Blackledge et al proposed an approach based on manual thresholding completed by a GrowCut algorithm (with the inclusion of a Markow random field to limit the number of false positive voxels) and a final reviewing by an expert radiologist in order to segment bone metastases below the C4 vertebra.104 Other approaches based on machine learning are also investigated.129
These developments are still in their infancy. Further work is therefore required in order to develop mature imaging tools which will allow an accurate and automated extraction of morphological and functional markers. Furthermore lesion detection and segmentation problems have to be resolved. These problems are complex and they may require the combination of different segmentation algorithms (thresholding, region growing, clustering).
There are some concerns regarding the reproducibility of quantitative measurements derived from MRI protocols, in particular from the ADC coefficient. Chenevert et al observed excellent agreement in ADC values obtained from different MRI magnets (from different vendors) on water phantoms (ADC variability of 5 to 6%).130 Messiou et al demonstrated that in normal healthy volunteers, the coefficient of reproducibility of ADC was 14.8%.131 In patients with lung tumours, Weller et al evaluated the ADC variability between 4 to 10% depending on the institution/MRI vendor.132 According to the authors, ADC offers a robust measurement which is not critically affected by the post-processing softwares and shows a satisfactory reproducibility. Blackledge et al evaluated the inter-observer variability of two readers in quantifying WB-DWI parameters.133 The authors showed that there was an excellent inter- and intra-observer repeatability for estimates of global mean/median apparent diffusion coefficient.
According to the aforementioned studies, ADC measurements from different MRI magnets are comparable when a similar acquisition protocol is implemented. However, ADC reproducibility strongly depends on the quality of the MR examination post-processing. Centralizing the quantitative analysis in a single centre may help towards this target, while allowing the realization the MR examinations of the patient in different machines and institutions.
Imaging of lung parenchyma
MRI imaging of the lung parenchyma and as a result lung tumours and metastasis, have been limited and relatively complicated because of respiratory motion, low SNR due to low tissue proton density and rapid signal decay due to susceptibility artefacts at air-tissue interfaces.134–137 The use of signal averaging increases SNR but also acquisition times. Furthermore, SNR could be increased by using larger voxel sizes but this would compromise the detection of smaller lung lesions because of partial volume effects.
In 2003 Biederer et al evaluated the diagnostic accuracy of different MR sequences for the detection of small artificial pulmonary nodules inside porcine lungs.138 3D and 2D GRE sequences demonstrated a sensitivity of 88% for 4 mm nodules. T2 weighted FSE and T2 weighted half Fourier single-shot sequences (T2-HASTE) were slightly inferior. For lesions larger than 5 mm, the sensitivity, specificity and positive and negative predictive values of all sequences except T2 weighted HASTE were close to 100%. The authors concluded that common MR imaging sequences have a high diagnostic accuracy in detecting small pulmonary nodules when cardiac and respiratory artefacts do not occur.
Parallel imaging and better respiratory gating techniques ameliorated significantly the MRI in lung imaging.136 Ultra-short echo time sequence for the imaging of lung parenchyma acquires signal at microseconds and reduces susceptibility artefacts.134, 139 This sequence allows to collect data almost immediately after excitation and thus only a limited amount of T2 and T2* signal decay occurs.139
Conclusion
WB-MRI has proven to be an effective tool for imaging of oncological patients. This non-irradiating technique is emerging from the research field and becoming a commonly used imaging tool thanks to the increasing availability of MRI. Recent studies have convincingly demonstrated that WB-MRI can be used for treatment monitoring and prognosis and can spare patients a battery of cumbersome examinations. New or old sequences that are revisited, as the Dixon imaging, improve tumoral lesion conspicuity and demonstrate encouraging results for shortened acquisition times. There is, however, an urgent need for standardization of WB-MRI protocols. New steps towards the homogenization of WB-MRI acquisitions, interpretation and reporting have been made in order to achieve the—urgently—required uniformity. Of course, all these technological advances moved the field forward in tremendous leaps and bounds and radiologists have to follow by acquiring skills in order to implement and interpret WB-MRI examinations. This very ambitious technique stands firm under the spotlight of evolving research, driving continuous improvements in the technique and guiding the way towards future directions and applications.
Contributor Information
Vassiliki Pasoglou, Email: vassiliki.pasoglou@uclouvain.be.
Nicolas Michoux, Email: nicolas.michoux@uclouvain.be.
Ahmed Larbi, Email: larbi.ahmed@gmail.com.
Sandy Van Nieuwenhove, Email: sandy.vannieuwenhove@uclouvain.be.
Frédéric Lecouvet, Email: frederic.lecouvet@uclouvain.be.
REFERENCES
- 1.Takahara T, Imai Y, Yamashita T, Yasuda S, Nasu S, Van Cauteren M. Diffusion weighted whole body imaging with background body signal suppression (DWIBS): technical improvement using free breathing, STIR and high resolution 3D display. Radiat Med 2004; 22: 275–82. [PubMed] [Google Scholar]
 - 2.Padhani AR, Liu G, Koh DM, Chenevert TL, Thoeny HC, Takahara T, et al. Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia 2009; 11: 102–25. doi: 10.1593/neo.81328 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 3.Lecouvet FE. Whole-body MR imaging: musculoskeletal applications. Radiology 2016; 279: 345–65. doi: 10.1148/radiol.2016142084 [DOI] [PubMed] [Google Scholar]
 - 4.Wu LM, Gu HY, Zheng J, Xu X, Lin LH, Deng X, et al. Diagnostic value of whole-body magnetic resonance imaging for bone metastases: a systematic review and meta-analysis. J Magn Reson Imaging 2011; 34: 128–35. doi: 10.1002/jmri.22608 [DOI] [PubMed] [Google Scholar]
 - 5.Fischer MA, Nanz D, Hany T, Reiner CS, Stolzmann P, Donati OF, et al. Diagnostic accuracy of whole-body MRI/DWI image fusion for detection of malignant tumours: a comparison with PET/CT. Eur Radiol 2011; 21: 246–55. doi: 10.1007/s00330-010-1929-x [DOI] [PubMed] [Google Scholar]
 - 6.Lecouvet FE, El Mouedden J, Collette L, Coche E, Danse E, Jamar F, et al. Can whole-body magnetic resonance imaging with diffusion-weighted imaging replace Tc 99m bone scanning and computed tomography for single-step detection of metastases in patients with high-risk prostate cancer? Eur Urol 2012; 62: 68–75. doi: 10.1016/j.eururo.2012.02.020 [DOI] [PubMed] [Google Scholar]
 - 7.Pasoglou V, Larbi A, Collette L, Annet L, Jamar F, Machiels JP, et al. One-step TNM staging of high-risk prostate cancer using magnetic resonance imaging (MRI): toward an upfront simplified “all-in-one” imaging approach? Prostate 2014; 74: 469–77. doi: 10.1002/pros.22764 [DOI] [PubMed] [Google Scholar]
 - 8.Tombal B, Lecouvet F. Modern detection of prostate cancer’s bone metastasis: is the bone scan era over? Adv Urol 2012; 2012: 1–8. doi: 10.1155/2012/893193 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 9.Engelhard K, Hollenbach HP, Wohlfart K, von Imhoff E, Fellner FA. Comparison of whole-body MRI with automatic moving table technique and bone scintigraphy for screening for bone metastases in patients with breast cancer. Eur Radiol 2004; 14: 99–105. doi: 10.1007/s00330-003-1968-7 [DOI] [PubMed] [Google Scholar]
 - 10.Gutzeit A, Doert A, Froehlich JM, Eckhardt BP, Meili A, Scherr P, et al. Comparison of diffusion-weighted whole body MRI and skeletal scintigraphy for the detection of bone metastases in patients with prostate or breast carcinoma. Skeletal Radiol 2010; 39: 333–43. doi: 10.1007/s00256-009-0789-4 [DOI] [PubMed] [Google Scholar]
 - 11.Schmidt GP, Baur-Melnyk A, Haug A, Utzschneider S, Becker CR, Tiling R, et al. Whole-body MRI at 1.5 T and 3 T compared with FDG-PET-CT for the detection of tumour recurrence in patients with colorectal cancer. Eur Radiol 2009; 19: 1366–78. doi: 10.1007/s00330-008-1289-y [DOI] [PubMed] [Google Scholar]
 - 12.Kosmin M, Makris A, Joshi PV, Ah-See ML, Woolf D, Padhani AR. The addition of whole-body magnetic resonance imaging to body computerised tomography alters treatment decisions in patients with metastatic breast cancer. Eur J Cancer 2017; 77: 109–16. doi: 10.1016/j.ejca.2017.03.001 [DOI] [PubMed] [Google Scholar]
 - 13.Schmidt GP, Baur-Melnyk A, Herzog P, Schmid R, Tiling R, Schmidt M, et al. High-resolution whole-body magnetic resonance image tumor staging with the use of parallel imaging versus dual-modality positron emission tomography-computed tomography: experience on a 32-channel system. Invest Radiol 2005; 40: 743–53. doi: 10.1097/01.rli.0000185878.61270.b0 [DOI] [PubMed] [Google Scholar]
 - 14.Schmidt GP, Baur-Melnyk A, Haug A, Heinemann V, Bauerfeind I, Reiser MF, et al. Comprehensive imaging of tumor recurrence in breast cancer patients using whole-body MRI at 1.5 and 3 T compared to FDG-PET-CT. Eur J Radiol 2008; 65: 47–58. doi: 10.1016/j.ejrad.2007.10.021 [DOI] [PubMed] [Google Scholar]
 - 15.Ohno Y, Koyama H, Nogami M, Takenaka D, Yoshikawa T, Yoshimura M, et al. Whole-body MR imaging vs. FDG-PET: comparison of accuracy of M-stage diagnosis for lung cancer patients. J Magn Reson Imaging 2007; 26: 498–509. doi: 10.1002/jmri.21031 [DOI] [PubMed] [Google Scholar]
 - 16.Ohno Y, Yoshikawa T, Kishida Y, Seki S, Koyama H, Yui M, et al. Diagnostic performance of different imaging modalities in the assessment of distant metastasis and local recurrence of tumor in patients with non-small cell lung cancer. J Magn Reson Imaging 2017; 46: 1707–17. doi: 10.1002/jmri.25726 [DOI] [PubMed] [Google Scholar]
 - 17.Shen G, Deng H, Hu S, Jia Z. Comparison of choline-PET/CT, MRI, SPECT, and bone scintigraphy in the diagnosis of bone metastases in patients with prostate cancer: a meta-analysis. Skeletal Radiol 2014; 43: 1503–13. doi: 10.1007/s00256-014-1903-9 [DOI] [PubMed] [Google Scholar]
 - 18.Conde-Moreno AJ, Herrando-Parreño G, Muelas-Soria R, Ferrer-Rebolleda J, Broseta-Torres R, Cozar-Santiago MP, et al. Whole-body diffusion-weighted magnetic resonance imaging (WB-DW-MRI) vs choline-positron emission tomography-computed tomography (choline-PET/CT) for selecting treatments in recurrent prostate cancer. Clin Transl Oncol 2017; 19: 553–61. doi: 10.1007/s12094-016-1563-4 [DOI] [PubMed] [Google Scholar]
 - 19.Wieder H, Beer AJ, Holzapfel K, Henninger M, Maurer T, Schwarzenboeck S, et al. 11C-choline PET/CT and whole-body MRI including diffusion-weighted imaging for patients with recurrent prostate cancer. Oncotarget 2017; 8: 66516–27. doi: 10.18632/oncotarget.16227 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 20.Ghosh A, Heston WD. Tumor target prostate specific membrane antigen (PSMA) and its regulation in prostate cancer. J Cell Biochem 2004; 91: 528–39. doi: 10.1002/jcb.10661 [DOI] [PubMed] [Google Scholar]
 - 21.Afshar-Oromieh A, Zechmann CM, Malcher A, Eder M, Eisenhut M, Linhart HG, et al. Comparison of PET imaging with a 68Ga-labelled PSMA ligand and 18F-choline-based PET/CT for the diagnosis of recurrent prostate cancer. Eur J Nucl Med Mol Imaging 2014; 41: 11–20. doi: 10.1007/s00259-013-2525-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 22.Afshar-Oromieh A, Haberkorn U, Hadaschik B, Habl G, Eder M, Eisenhut M, et al. PET/MRI with a 68Ga-PSMA ligand for the detection of prostate cancer. Eur J Nucl Med Mol Imaging 2013; 40: 1629–30. doi: 10.1007/s00259-013-2489-5 [DOI] [PubMed] [Google Scholar]
 - 23.Gupta M, Choudhury PS, Hazarika D, Rawal S. A comparative study of 68gallium-prostate specific membrane antigen positron emission tomography-computed tomography and magnetic resonance imaging for lymph node staging in high risk prostate cancer patients: an initial experience. World J Nucl Med 2017; 16: 186–91. doi: 10.4103/1450-1147.207272 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 24.Afshar-Oromieh A, Avtzi E, Giesel FL, Holland-Letz T, Linhart HG, Eder M, et al. The diagnostic value of PET/CT imaging with the 68Ga-labelled PSMA ligand HBED-CC in the diagnosis of recurrent prostate cancer. Eur J Nucl Med Mol Imaging 2015; 42: 197–209. doi: 10.1007/s00259-014-2949-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 25.Öbek C, Doğanca T, Demirci E, Ocak M, Kural AR, Yıldırım A, et al. The accuracy of 68Ga-PSMA PET/CT in primary lymph node staging in high-risk prostate cancer. Eur J Nucl Med Mol Imaging 2017; 44: 1806–12. doi: 10.1007/s00259-017-3752-y [DOI] [PubMed] [Google Scholar]
 - 26.Mottet N, Bellmunt J, Bolla M, Briers E, Cumberbatch MG, De Santis M, et al. EAU-ESTRO-SIOG guidelines on prostate cancer. Part 1: screening, diagnosis, and local treatment with curative intent. Eur Urol 2017; 71: 618–29. doi: 10.1016/j.eururo.2016.08.003 [DOI] [PubMed] [Google Scholar]
 - 27.Albers P, Albrecht W, Algaba F, Bokemeyer C, Cohn-Cedermark G, Fizazi K, et al. EAU guidelines on testicular cancer: 2011 update. European association of urology. Actas Urol Esp 2012; 36: 127–45. doi: 10.1016/j.acuro.2011.06.017 [DOI] [PubMed] [Google Scholar]
 - 28.van As NJ, Gilbert DC, Money-Kyrle J, Bloomfield D, Beesley S, Dearnaley DP, et al. Evidence-based pragmatic guidelines for the follow-up of testicular cancer: optimising the detection of relapse. Br J Cancer 2008; 98: 1894–902. doi: 10.1038/sj.bjc.6604280 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 29.Mosavi F, Laurell A, Ahlström H. Whole body MRI, including diffusion-weighted imaging in follow-up of patients with testicular cancer. Acta Oncol 2015; 54: 1763–9. doi: 10.3109/0284186X.2015.1043027 [DOI] [PubMed] [Google Scholar]
 - 30.Sohaib SA, Koh DM, Barbachano Y, Parikh J, Husband JE, Dearnaley DP, et al. Prospective assessment of MRI for imaging retroperitoneal metastases from testicular germ cell tumours. Clin Radiol 2009; 64: 362–7. doi: 10.1016/j.crad.2008.10.011 [DOI] [PubMed] [Google Scholar]
 - 31.Ruf J, Heuck F, Schiefer J, Denecke T, Elgeti F, Pascher A, et al. Impact of Multiphase 68Ga-DOTATOC-PET/CT on therapy management in patients with neuroendocrine tumors. Neuroendocrinology 2010; 91: 101–9. doi: 10.1159/000265561 [DOI] [PubMed] [Google Scholar]
 - 32.Buchmann I, Henze M, Engelbrecht S, Eisenhut M, Runz A, Schäfer M, et al. Comparison of 68Ga-DOTATOC PET and 111In-DTPAOC (Octreoscan) SPECT in patients with neuroendocrine tumours. Eur J Nucl Med Mol Imaging 2007; 34: 1617–26. doi: 10.1007/s00259-007-0450-1 [DOI] [PubMed] [Google Scholar]
 - 33.Kwekkeboom DJ, Kam BL, van Essen M, Teunissen JJ, van Eijck CH, Valkema R, et al. Somatostatin-receptor-based imaging and therapy of gastroenteropancreatic neuroendocrine tumors. Endocr Relat Cancer 2010; 17: R53–R73. doi: 10.1677/ERC-09-0078 [DOI] [PubMed] [Google Scholar]
 - 34.Carlbom L, Caballero-Corbalán J, Granberg D, Sörensen J, Eriksson B, Ahlström H. Whole-body MRI including diffusion-weighted MRI compared with 5-HTP PET/CT in the detection of neuroendocrine tumors. Ups J Med Sci 2017; 122: 43–50. doi: 10.1080/03009734.2016.1248803 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 35.Etchebehere EC, de Oliveira Santos A, Gumz B, Vicente A, Hoff PG, Corradi G, et al. 68Ga-DOTATATE PET/CT, 99mTc-HYNIC-octreotide SPECT/CT, and whole-body MR imaging in detection of neuroendocrine tumors: a prospective trial. J Nucl Med 2014; 55: 1598–604. doi: 10.2967/jnumed.114.144543 [DOI] [PubMed] [Google Scholar]
 - 36.Moryoussef F, de Mestier L, Belkebir M, Deguelte-Lardière S, Brixi H, Kianmanesh R, et al. Impact of liver and whole-body diffusion-weighted MRI for neuroendocrine tumors on patient management: a pilot study. Neuroendocrinology 2017; 104: 264–72. doi: 10.1159/000446369 [DOI] [PubMed] [Google Scholar]
 - 37.Müller-Horvat C, Radny P, Eigentler TK, Schäfer J, Pfannenberg C, Horger M, et al. Prospective comparison of the impact on treatment decisions of whole-body magnetic resonance imaging and computed tomography in patients with metastatic malignant melanoma. Eur J Cancer 2006; 42: 342–50. doi: 10.1016/j.ejca.2005.10.008 [DOI] [PubMed] [Google Scholar]
 - 38.Pfannenberg C, Aschoff P, Schanz S, Eschmann SM, Plathow C, Eigentler TK, et al. Prospective comparison of 18F-fluorodeoxyglucose positron emission tomography/computed tomography and whole-body magnetic resonance imaging in staging of advanced malignant melanoma. Eur J Cancer 2007; 43: 557–64. doi: 10.1016/j.ejca.2006.11.014 [DOI] [PubMed] [Google Scholar]
 - 39.Laurent V, Trausch G, Bruot O, Olivier P, Felblinger J, Régent D. Comparative study of two whole-body imaging techniques in the case of melanoma metastases: advantages of multi-contrast MRI examination including a diffusion-weighted sequence in comparison with PET-CT. Eur J Radiol 2010; 75: 376–83. doi: 10.1016/j.ejrad.2009.04.059 [DOI] [PubMed] [Google Scholar]
 - 40.Petralia G, Padhani A, Summers P, Alessi S, Raimondi S, Testori A, et al. Whole-body diffusion-weighted imaging: is it all we need for detecting metastases in melanoma patients? Eur Radiol 2013; 23: 3466–76. doi: 10.1007/s00330-013-2968-x [DOI] [PubMed] [Google Scholar]
 - 41.Pflugfelder A, Kochs C, Blum A, Capellaro M, Czeschik C, Dettenborn T, et al. Malignant melanoma S3-guideline “diagnosis, therapy and follow-up of melanoma”. J Dtsch Dermatol Ges 2013; 11(Suppl 6): 1–116. doi: 10.1111/ddg.12113_suppl [DOI] [PubMed] [Google Scholar]
 - 42.Dummer R, Siano M, Hunger RE, Lindenblatt N, Braun R, Michielin O, et al. The updated Swiss guidelines 2016 for the treatment and follow-up of cutaneous melanoma. Swiss Med Wkly 2016; 146: w14279. doi: 10.4414/smw.2016.14279 [DOI] [PubMed] [Google Scholar]
 - 43.Zamagni E, Nanni C, Patriarca F, Englaro E, Castellucci P, Geatti O, et al. A prospective comparison of 18F-fluorodeoxyglucose positron emission tomography-computed tomography, magnetic resonance imaging and whole-body planar radiographs in the assessment of bone disease in newly diagnosed multiple myeloma. Haematologica 2007; 92: 50–5. doi: 10.3324/haematol.10554 [DOI] [PubMed] [Google Scholar]
 - 44.Gleeson TG, Moriarty J, Shortt CP, Gleeson JP, Fitzpatrick P, Byrne B, et al. Accuracy of whole-body low-dose multidetector CT (WBLDCT) versus skeletal survey in the detection of myelomatous lesions, and correlation of disease distribution with whole-body MRI (WBMRI). Skeletal Radiol 2009; 38: 225–36. doi: 10.1007/s00256-008-0607-4 [DOI] [PubMed] [Google Scholar]
 - 45.Dimopoulos MA, Hillengass J, Usmani S, Zamagni E, Lentzsch S, Davies FE, et al. Role of magnetic resonance imaging in the management of patients with multiple myeloma: a consensus statement. J Clin Oncol 2015; 33: 657–64. doi: 10.1200/JCO.2014.57.9961 [DOI] [PubMed] [Google Scholar]
 - 46.Excellence, N.N.I.f.H.a.C. Myeloma: diagnosis and management NICE guideline [NG35]. 2016. Available from: https://www.nice.org.uk/guidance/ng35
 - 47.Chantry A, Kazmi M, Barrington S, Goh V, Mulholland N, Streetly M, et al. Guidelines for the use of imaging in the management of patients with myeloma. Br J Haematol 2017; 178: 380–93. doi: 10.1111/bjh.14827 [DOI] [PubMed] [Google Scholar]
 - 48.Bäuerle T, Hillengass J, Fechtner K, Zechmann CM, Grenacher L, Moehler TM, et al. Multiple myeloma and monoclonal gammopathy of undetermined significance: importance of whole-body versus spinal MR imaging. Radiology 2009; 252: 477–85. doi: 10.1148/radiol.2522081756 [DOI] [PubMed] [Google Scholar]
 - 49.Rasche L, Angtuaco E, McDonald JE, Buros A, Stein C, Pawlyn C, et al. Low expression of hexokinase-2 is associated with false-negative FDG-positron emission tomography in multiple myeloma. Blood 2017; 130: 30–4. doi: 10.1182/blood-2017-03-774422 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 50.Dixon WT. Simple proton spectroscopic imaging. Radiology 1984; 153: 189–94. doi: 10.1148/radiology.153.1.6089263 [DOI] [PubMed] [Google Scholar]
 - 51.Bray TJP, Singh S, Latifoltojar A, Rajesparan K, Rahman F, Narayanan P, et al. Diagnostic utility of whole body Dixon MRI in multiple myeloma: a multi-reader study. PLoS One 2017; 12: e0180562. doi: 10.1371/journal.pone.0180562 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 52.Carbone PP, Kaplan HS, Musshoff K, Smithers DW, Tubiana M. Report of the committee on hodgkin’s disease staging classification. Cancer Res 1971; 31: 1860–1. [PubMed] [Google Scholar]
 - 53.Lister TA, Crowther D, Sutcliffe SB, Glatstein E, Canellos GP, Young RC, et al. Report of a committee convened to discuss the evaluation and staging of patients with hodgkin’s disease: cotswolds meeting. J Clin Oncol 1989; 7: 1630–6. doi: 10.1200/JCO.1989.7.11.1630 [DOI] [PubMed] [Google Scholar]
 - 54.Wang J, Weiss LM, Chang KL, Slovak ML, Gaal K, Forman SJ, et al. Diagnostic utility of bilateral bone marrow examination: significance of morphologic and ancillary technique study in malignancy. Cancer 2002; 94: 1522–31. [DOI] [PubMed] [Google Scholar]
 - 55.Haddy TB, Parker RI, Magrath IT. Bone marrow involvement in young patients with non-hodgkin’s lymphoma: the importance of multiple bone marrow samples for accurate staging. Med Pediatr Oncol 1989; 17: 418–23. doi: 10.1002/mpo.2950170512 [DOI] [PubMed] [Google Scholar]
 - 56.Coller BS, Chabner BA, Gralnick HR. Frequencies and patterns of bone marrow involvement in non-Hodgkin lymphomas: observations on the value of bilateral biopsies. Am J Hematol 1977; 3: 105–19. doi: 10.1002/ajh.2830030201 [DOI] [PubMed] [Google Scholar]
 - 57.Connors JM. State-of-the-art therapeutics: hodgkin’s lymphoma. J Clin Oncol 2005; 23: 6400–8. doi: 10.1200/JCO.2005.05.016 [DOI] [PubMed] [Google Scholar]
 - 58.Punwani S, Taylor SA, Saad ZZ, Bainbridge A, Groves A, Daw S, et al. Diffusion-weighted MRI of lymphoma: prognostic utility and implications for PET/MRI? Eur J Nucl Med Mol Imaging 2013; 40: 373–85. doi: 10.1007/s00259-012-2293-7 [DOI] [PubMed] [Google Scholar]
 - 59.Adams HJ, Kwee TC, Lokhorst HM, Westerweel PE, Fijnheer R, Kersten MJ, et al. Potential prognostic implications of whole-body bone marrow MRI in diffuse large B-cell lymphoma patients with a negative blind bone marrow biopsy. J Magn Reson Imaging 2014; 39: 1394–400. doi: 10.1002/jmri.24318 [DOI] [PubMed] [Google Scholar]
 - 60.Albano D, Patti C, Lagalla R, Midiri M, Galia M. Whole-body MRI, FDG-PET/CT, and bone marrow biopsy, for the assessment of bone marrow involvement in patients with newly diagnosed lymphoma. J Magn Reson Imaging 2017; 45: 1082–9. doi: 10.1002/jmri.25439 [DOI] [PubMed] [Google Scholar]
 - 61.Tsunoda S, Takagi S, Tanaka O, Miura Y. Clinical and prognostic significance of femoral marrow magnetic resonance imaging in patients with malignant lymphoma. Blood 1997; 89: 286–90. [PubMed] [Google Scholar]
 - 62.Jerusalem G, Beguin Y, Najjar F, Hustinx R, Fassotte MF, Rigo P, et al. Positron emission tomography (PET) with 18F-fluorodeoxyglucose (18F-FDG) for the staging of low-grade non-hodgkin’s lymphoma (NHL). Ann Oncol 2001; 12: 825–30. doi: 10.1023/A:1011169332265 [DOI] [PubMed] [Google Scholar]
 - 63.Karam M, Novak L, Cyriac J, Ali A, Nazeer T, Nugent F. Role of fluorine-18 fluoro-deoxyglucose positron emission tomography scan in the evaluation and follow-up of patients with low-grade lymphomas. Cancer 2006; 107: 175–83. doi: 10.1002/cncr.21967 [DOI] [PubMed] [Google Scholar]
 - 64.Elstrom R, Guan L, Baker G, Nakhoda K, Vergilio JA, Zhuang H, et al. Utility of FDG-PET scanning in lymphoma by WHO classification. Blood 2003; 101: 3875–6. doi: 10.1182/blood-2002-09-2778 [DOI] [PubMed] [Google Scholar]
 - 65.Ray JG, Vermeulen MJ, Bharatha A, Montanera WJ, Park AL. Association between MRI exposure during pregnancy and fetal and childhood outcomes. JAMA 2016; 316: 952–61. doi: 10.1001/jama.2016.12126 [DOI] [PubMed] [Google Scholar]
 - 66.Villani A, Tabori U, Schiffman J, Shlien A, Beyene J, Druker H, et al. Biochemical and imaging surveillance in germline TP53 mutation carriers with Li-Fraumeni syndrome: a prospective observational study. Lancet Oncol 2011; 12: 559–67. doi: 10.1016/S1470-2045(11)70119-X [DOI] [PubMed] [Google Scholar]
 - 67.Monsalve J, Kapur J, Malkin D, Babyn PS. Imaging of cancer predisposition syndromes in children. Radiographics 2011; 31: 263–80. doi: 10.1148/rg.311105099 [DOI] [PubMed] [Google Scholar]
 - 68.Friedman DN, Lis E, Sklar CA, Oeffinger KC, Reppucci M, Fleischut MH, et al. Whole-body magnetic resonance imaging (WB-MRI) as surveillance for subsequent malignancies in survivors of hereditary retinoblastoma: a pilot study. Pediatr Blood Cancer 2014; 61: 1440–4. doi: 10.1002/pbc.24835 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 69.Anupindi SA, Bedoya MA, Lindell RB, Rambhatla SJ, Zelley K, Nichols KE, et al. Diagnostic performance of whole-body MRI as a tool for cancer screening in children with genetic cancer-predisposing conditions. AJR Am J Roentgenol 2015; 205: 400–8. doi: 10.2214/AJR.14.13663 [DOI] [PubMed] [Google Scholar]
 - 70.Ballinger ML, Best A, Mai PL, Khincha PP, Loud JT, Peters JA, et al. Baseline surveillance in Li-Fraumeni syndrome using whole-body magnetic resonance imaging: a meta-analysis. JAMA Oncol 2017; 3: 1634–9. doi: 10.1001/jamaoncol.2017.1968 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 71.Goo HW, Yang DH, Ra YS, Song JS, Im HJ, Seo JJ, et al. Whole-body MRI of Langerhans cell histiocytosis: comparison with radiography and bone scintigraphy. Pediatr Radiol 2006; 36: 1019–31. doi: 10.1007/s00247-006-0246-7 [DOI] [PubMed] [Google Scholar]
 - 72.Hardes J, Gosheger G. Advantages in vascular tumors. Dtsch Arztebl Int 2010; 107: 750. doi: 10.3238/arztebl.2010.0750 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 73.Jasperson KW, Kohlmann W, Gammon A, Slack H, Buchmann L, Hunt J, et al. Role of rapid sequence whole-body MRI screening in SDH-associated hereditary paraganglioma families. Fam Cancer 2014; 13: 257: 257–65. doi: 10.1007/s10689-013-9639-6 [DOI] [PubMed] [Google Scholar]
 - 74.Koh DM, Blackledge M, Padhani AR, Takahara T, Kwee TC, Leach MO, et al. Whole-body diffusion-weighted MRI: tips, tricks, and pitfalls. AJR Am J Roentgenol 2012; 199: 252–62. doi: 10.2214/AJR.11.7866 [DOI] [PubMed] [Google Scholar]
 - 75.Pasoglou V, Michoux N, Tombal B, Jamar F, Lecouvet FE. wbMRI to detect bone metastases: critical review on diagnostic accuracy and comparison to other imaging modalities. Clin Transl Imaging 2015; 3: 141–57. doi: 10.1007/s40336-015-0120-4 [DOI] [Google Scholar]
 - 76.Balliu E, Boada M, Peláez I, Vilanova JC, Barceló-Vidal C, Rubio A, et al. Comparative study of whole-body MRI and bone scintigraphy for the detection of bone metastases. Clin Radiol 2010; 65: 989–96. doi: 10.1016/j.crad.2010.07.002 [DOI] [PubMed] [Google Scholar]
 - 77.Nakanishi K, Kobayashi M, Nakaguchi K, Kyakuno M, Hashimoto N, Onishi H, et al. Whole-body MRI for detecting metastatic bone tumor: diagnostic value of diffusion-weighted images. Magn Reson Med Sci 2007; 6: 147–55. doi: 10.2463/mrms.6.147 [DOI] [PubMed] [Google Scholar]
 - 78.Eustace S, Tello R, DeCarvalho V, Carey J, Wroblicka JT, Melhem ER, et al. A comparison of whole-body turboSTIR MR imaging and planar 99mTc-methylene diphosphonate scintigraphy in the examination of patients with suspected skeletal metastases. AJR Am J Roentgenol 1997; 169: 1655–61. doi: 10.2214/ajr.169.6.9393186 [DOI] [PubMed] [Google Scholar]
 - 79.Mosavi F, Johansson S, Sandberg DT, Turesson I, Sörensen J, Ahlström H. Whole-body diffusion-weighted MRI compared with 18F-NaF PET/CT for detection of bone metastases in patients with high-risk prostate carcinoma. AJR Am J Roentgenol 2012; 199: 1114–20. doi: 10.2214/AJR.11.8351 [DOI] [PubMed] [Google Scholar]
 - 80.Lecouvet FE, Lhommel R, Pasoglou V, Larbi A, Jamar F, Tombal B. Novel imaging techniques reshape the landscape in high-risk prostate cancers. Curr Opin Urol 2013; 23: 323–30. doi: 10.1097/MOU.0b013e328361d451 [DOI] [PubMed] [Google Scholar]
 - 81.Schmidt GP, Paprottka P, Jakobs TF, Hoffmann RT, Baur-Melnyk A, Haug A, et al. FDG-PET-CT and whole-body MRI for triage in patients planned for radioembolisation therapy. Eur J Radiol 2012; 81: e269–e276. doi: 10.1016/j.ejrad.2011.02.018 [DOI] [PubMed] [Google Scholar]
 - 82.Ghanem N, Altehoefer C, Kelly T, Lohrmann C, Winterer J, Schäfer O, et al. Whole-body MRI in comparison to skeletal scintigraphy in detection of skeletal metastases in patients with solid tumors. In Vivo 2006; 20: 173–82. [PubMed] [Google Scholar]
 - 83.Walker R, Kessar P, Blanchard R, Dimasi M, Harper K, DeCarvalho V, et al. Turbo STIR magnetic resonance imaging as a whole-body screening tool for metastases in patients with breast carcinoma: preliminary clinical experience. J Magn Reson Imaging 2000; 11: 343–50. doi: [DOI] [PubMed] [Google Scholar]
 - 84.Latifoltojar A, Hall-Craggs M, Bainbridge A, Rabin N, Popat R, Rismani A, et al. Whole-body MRI quantitative biomarkers are associated significantly with treatment response in patients with newly diagnosed symptomatic multiple myeloma following bortezomib induction. Eur Radiol 2017; 27: 5325–36. doi: 10.1007/s00330-017-4907-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 85.Del Grande F, Santini F, Herzka DA, Aro MR, Dean CW, Gold GE, et al. Fat-suppression techniques for 3-T MR imaging of the musculoskeletal system. Radiographics 2014; 34: 217–33. doi: 10.1148/rg.341135130 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 86.Ma J, Costelloe CM, Madewell JE, Hortobagyi GN, Green MC, Cao G, et al. Fast dixon-based multisequence and multiplanar MRI for whole-body detection of cancer metastases. J Magn Reson Imaging 2009; 29: 1154–62. doi: 10.1002/jmri.21746 [DOI] [PubMed] [Google Scholar]
 - 87.Costelloe CM, Kundra V, Ma J, Chasen BA, Rohren EM, Bassett RL, et al. Fast Dixon whole-body MRI for detecting distant cancer metastasis: a preliminary clinical study. J Magn Reson Imaging 2012; 35: 399–408. doi: 10.1002/jmri.22815 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 88.Costelloe CM, Madewell JE, Kundra V, Harrell RK, Bassett RL, Ma J. Conspicuity of bone metastases on fast Dixon-based multisequence whole-body MRI: clinical utility per sequence. Magn Reson Imaging 2013; 31: 669–75. doi: 10.1016/j.mri.2012.10.017 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 89.Latifoltojar A, Hall-Craggs M, Rabin N, Popat R, Bainbridge A, Dikaios N, et al. Whole body magnetic resonance imaging in newly diagnosed multiple myeloma: early changes in lesional signal fat fraction predict disease response. Br J Haematol 2017; 176: 222–33. doi: 10.1111/bjh.14401 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 90.Messiou C, Giles S, Collins DJ, West S, Davies FE, Morgan GJ, et al. Assessing response of myeloma bone disease with diffusion-weighted MRI. Br J Radiol 2012; 85: e1198–e1203. doi: 10.1259/bjr/52759767 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 91.Takasu M, Kaichi Y, Tani C, Date S, Akiyama Y, Kuroda Y, et al. Iterative decomposition of water and fat with echo asymmetry and least-squares estimation (IDEAL) magnetic resonance imaging as a biomarker for symptomatic multiple myeloma. PLoS One 2015; 10: e0116842. doi: 10.1371/journal.pone.0116842 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 92.Berglund J, Johansson L, Ahlström H, Kullberg J. Three-point Dixon method enables whole-body water and fat imaging of obese subjects. Magn Reson Med 2010; 63: 1659–68. doi: 10.1002/mrm.22385 [DOI] [PubMed] [Google Scholar]
 - 93.Shortt CP, Gleeson TG, Breen KA, McHugh J, O'Connell MJ, O'Gorman PJ, et al. Whole-body MRI versus PET in assessment of multiple myeloma disease activity. AJR Am J Roentgenol 2009; 192: 980–6. doi: 10.2214/AJR.08.1633 [DOI] [PubMed] [Google Scholar]
 - 94.Krohmer S, Sorge I, Krausse A, Kluge R, Bierbach U, Marwede D, et al. Whole-body MRI for primary evaluation of malignant disease in children. Eur J Radiol 2010; 74: 256–61. doi: 10.1016/j.ejrad.2009.01.037 [DOI] [PubMed] [Google Scholar]
 - 95.Pasoglou V, Michoux N, Peeters F, Larbi A, Tombal B, Selleslagh T, et al. Whole-body 3D T1-weighted MR imaging in patients with prostate cancer: feasibility and evaluation in screening for metastatic disease. Radiology 2015; 275: 155–66. doi: 10.1148/radiol.14141242 [DOI] [PubMed] [Google Scholar]
 - 96.Padhani AR, Lecouvet FE, Tunariu N, Koh DM, De Keyzer F, Collins DJ, et al. METastasis Reporting and data system for prostate cancer: practical guidelines for acquisition, interpretation, and reporting of whole-body magnetic resonance imaging-based evaluations of multiorgan involvement in advanced prostate cancer. Eur Urol 2017; 71: 81–92. doi: 10.1016/j.eururo.2016.05.033 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 97.Ohlmann-Knafo S, Tarnoki AD, Tarnoki DL, Pickuth D. MR diagnosis of bone metastases at 1.5 T and 3 T: Can STIR imaging be omitted? Rofo 2015; 187: 924–32. doi: 10.1055/s-0035-1553207 [DOI] [PubMed] [Google Scholar]
 - 98.Horger M, Weisel K, Horger W, Mroue A, Fenchel M, Lichy M. Whole-body diffusion-weighted MRI with apparent diffusion coefficient mapping for early response monitoring in multiple myeloma: preliminary results. AJR Am J Roentgenol 2011; 196: W790–W795. doi: 10.2214/AJR.10.5979 [DOI] [PubMed] [Google Scholar]
 - 99.Messiou C, deSouza NM. Diffusion Weighted Magnetic Resonance Imaging of metastatic bone disease: a biomarker for treatment response monitoring. Cancer Biomark 2010; 6: 21–32. doi: 10.3233/CBM-2009-0116 [DOI] [PubMed] [Google Scholar]
 - 100.Lecouvet FE, Talbot JN, Messiou C, Bourguet P, Liu Y, de Souza NM. Monitoring the response of bone metastases to treatment with Magnetic Resonance Imaging and nuclear medicine techniques: a review and position statement by the European Organisation for Research and Treatment of Cancer imaging group. Eur J Cancer 2014; 50: 2519–31. doi: 10.1016/j.ejca.2014.07.002 [DOI] [PubMed] [Google Scholar]
 - 101.Merz M, Hielscher T, Wagner B, Sauer S, Shah S, Raab MS, et al. Predictive value of longitudinal whole-body magnetic resonance imaging in patients with smoldering multiple myeloma. Leukemia 2014; 28: 1902–8. doi: 10.1038/leu.2014.75 [DOI] [PubMed] [Google Scholar]
 - 102.Bannas P, Hentschel HB, Bley TA, Treszl A, Eulenburg C, Derlin T, et al. Diagnostic performance of whole-body MRI for the detection of persistent or relapsing disease in multiple myeloma after stem cell transplantation. Eur Radiol 2012; 22: 2007–12. doi: 10.1007/s00330-012-2445-y [DOI] [PubMed] [Google Scholar]
 - 103.Mayerhoefer ME, Karanikas G, Kletter K, Kiesewetter B, Weber M, Rausch I, et al. Can interim 18F-FDG PET or diffusion-weighted MRI predict end-of-treatment outcome in FDG-avid MALT lymphoma after rituximab-based therapy?: a preliminary study in 15 patients. Clin Nucl Med 2016; 41: 837–43. doi: 10.1097/RLU.0000000000001395 [DOI] [PubMed] [Google Scholar]
 - 104.Blackledge MD, Collins DJ, Tunariu N, Orton MR, Padhani AR, Leach MO, et al. Assessment of treatment response by total tumor volume and global apparent diffusion coefficient using diffusion-weighted MRI in patients with metastatic bone disease: a feasibility study. PLoS One 2014; 9: e91779: e91779. doi: 10.1371/journal.pone.0091779 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 105.Perez-Lopez R, Lorente D, Blackledge MD, Collins DJ, Mateo J, Bianchini D, et al. Volume of bone metastasis assessed with whole-body diffusion-weighted imaging is associated with overall survival in metastatic castration-resistant prostate cancer. Radiology 2016; 280: 151–60. doi: 10.1148/radiol.2015150799 [DOI] [PubMed] [Google Scholar]
 - 106.Perez-Lopez R, Mateo J, Mossop H, Blackledge MD, Collins DJ, Rata M, et al. Diffusion-weighted imaging as a treatment response biomarker for evaluating bone metastases in prostate cancer: a pilot study. Radiology 2017; 283: 168–77. doi: 10.1148/radiol.2016160646 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 107.Messiou C, Collins DJ, Giles S, de Bono JS, Bianchini D, de Souza NM. Assessing response in bone metastases in prostate cancer with diffusion weighted MRI. Eur Radiol 2011; 21: 2169–77. doi: 10.1007/s00330-011-2173-8 [DOI] [PubMed] [Google Scholar]
 - 108.Reischauer C, Froehlich JM, Koh DM, Graf N, Padevit C, John H, et al. Bone metastases from prostate cancer: assessing treatment response by using diffusion-weighted imaging and functional diffusion maps-initial observations. Radiology 2010; 257: 523–31. doi: 10.1148/radiol.10092469 [DOI] [PubMed] [Google Scholar]
 - 109.Hellman S, Weichselbaum RR. Oligometastases. J Clin Oncol 1995; 13: 8–10. doi: 10.1200/JCO.1995.13.1.8 [DOI] [PubMed] [Google Scholar]
 - 110.Network NCC. National comprehensive clinical guidelines: NCCN Clinical Practice Guidelines in Oncology . 2008. Available from: https://www.nccn.org/professionals/physician_gls/default.aspx.
 - 111.European School of Oncology (ESO)-MBC Task Force Metastatic breast cancer. Recommendations proposal from the European School of Oncology (ESO)-MBC Task Force. Breast 2007; 16: 9–10. [DOI] [PubMed] [Google Scholar]
 - 112.Gillessen S, Fanti S, Omlin A. panelists and authors of APCCC Reply to the letter to the editor “management of patients with advanced prostate cancer: recommendations of the St Gallen advanced prostate cancer consensus conference (APCCC) 2015” by Gillessen et al. Ann Oncol 2015; 26: 2354.2–5. doi: 10.1093/annonc/mdv360 [DOI] [PubMed] [Google Scholar]
 - 113.Gillessen S, Attard G, Beer TM, Beltran H, Bossi A, Bristow R, et al. Management of patients with advanced prostate cancer: the report of the advanced prostate cancer consensus conference APCCC 2017. Eur Urol 2018; 73: 178–211. doi: 10.1016/j.eururo.2017.06.002 [DOI] [PubMed] [Google Scholar]
 - 114.Ost P, Bossi A, Decaestecker K, De Meerleer G, Giannarini G, Karnes RJ, et al. Metastasis-directed therapy of regional and distant recurrences after curative treatment of prostate cancer: a systematic review of the literature. Eur Urol 2015; 67: 852–63. doi: 10.1016/j.eururo.2014.09.004 [DOI] [PubMed] [Google Scholar]
 - 115.Scher HI, Halabi S, Tannock I, Morris M, Sternberg CN, Carducci MA, et al. Design and end points of clinical trials for patients with progressive prostate cancer and castrate levels of testosterone: recommendations of the Prostate Cancer Clinical Trials Working Group. J Clin Oncol 2008; 26: 1148–59. doi: 10.1200/JCO.2007.12.4487 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 116.Larbi A, Dallaudière B, Pasoglou V, Padhani A, Michoux N, Vande Berg BC, et al. Whole body MRI (WB-MRI) assessment of metastatic spread in prostate cancer: therapeutic perspectives on targeted management of oligometastatic disease. Prostate 2016; 76: 1024–33. doi: 10.1002/pros.23196 [DOI] [PubMed] [Google Scholar]
 - 117.Antoch G, Vogt FM, Freudenberg LS, Nazaradeh F, Goehde SC, Barkhausen J, et al. Whole-body dual-modality PET/CT and whole-body MRI for tumor staging in oncology. JAMA 2003; 290: 3199–206. doi: 10.1001/jama.290.24.3199 [DOI] [PubMed] [Google Scholar]
 - 118.Heusner T, Gölitz P, Hamami M, Eberhardt W, Esser S, Forsting M, et al. “One-stop-shop” staging: should we prefer FDG-PET/CT or MRI for the detection of bone metastases? Eur J Radiol 2011; 78: 430–5. doi: 10.1016/j.ejrad.2009.10.031 [DOI] [PubMed] [Google Scholar]
 - 119.Robertson NL, Sala E, Benz M, Landa J, Scardino P, Scher HI, et al. Combined whole body and multiparametric prostate magnetic resonance imaging as a 1-step approach to the simultaneous assessment of local recurrence and metastatic disease after radical prostatectomy. J Urol 2017; 198: 65–70. doi: 10.1016/j.juro.2017.02.071 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 120.Griswold MA, Jakob PM, Heidemann RM, Nittka M, Jellus V, Wang J, et al. Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med 2002; 47: 1202–10. doi: 10.1002/mrm.10171 [DOI] [PubMed] [Google Scholar]
 - 121.Roemer PB, Edelstein WA, Hayes CE, Souza SP, Mueller OM. The NMR phased array. Magn Reson Med 1990; 16: 192–225. doi: 10.1002/mrm.1910160203 [DOI] [PubMed] [Google Scholar]
 - 122.Feinberg DA, Hale JD, Watts JC, Kaufman L, Mark A. Halving MR imaging time by conjugation: demonstration at 3.5 kG. Radiology 1986; 161: 527–31. doi: 10.1148/radiology.161.2.3763926 [DOI] [PubMed] [Google Scholar]
 - 123.Kuhl CK, Bruhn R, Krämer N, Nebelung S, Heidenreich A, Schrading S. Abbreviated biparametric prostate MR imaging in men with elevated prostate-specific antigen. Radiology 2017; 285: 493–505. doi: 10.1148/radiol.2017170129 [DOI] [PubMed] [Google Scholar]
 - 124.Fascelli M, Rais-Bahrami S, Sankineni S, Brown AM, George AK, Ho R, et al. Combined biparametric prostate magnetic resonance imaging and prostate-specific antigen in the detection of prostate cancer: a validation study in a biopsy-naive patient population. Urology 2016; 88: 125–34. doi: 10.1016/j.urology.2015.09.035 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 125.Turkbey B, Choyke PL. Prostate cancer: birth of a standard: MET-RADS-P for metastatic prostate cancer. Nat Rev Urol 2016; 13: 568–70. doi: 10.1038/nrurol.2016.163 [DOI] [PubMed] [Google Scholar]
 - 126.Dzyubachyk O, Staring M, Reijnierse M, Lelieveldt BP, van der Geest RJ. Inter-station intensity standardization for whole-body MR data. Magn Reson Med 2017; 77: 422–33. doi: 10.1002/mrm.26098 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 127.Dzyubachyk O, Blaas J, Botha CP, Staring M, Reijnierse M, Bloem JL, et al. Comparative exploration of whole-body MR through locally rigid transforms. Int J Comput Assist Radiol Surg 2013; 8: 635–47. doi: 10.1007/s11548-013-0820-z [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 128.Ceranka J, Polfliet M, Lecouvet F, Michoux N, de Mey J, Vandemeulebroucke J. Registration strategies for multi-modal whole-body MRI mosaicing. Magn Reson Med 2018; 79: 1684–95. doi: 10.1002/mrm.26787 [DOI] [PubMed] [Google Scholar]
 - 129.Wang S, Summers RM. Machine learning and radiology. Med Image Anal 2012; 16: 933–51. doi: 10.1016/j.media.2012.02.005 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 130.Chenevert TL, Galbán CJ, Ivancevic MK, Rohrer SE, Londy FJ, Kwee TC, et al. Diffusion coefficient measurement using a temperature-controlled fluid for quality control in multicenter studies. J Magn Reson Imaging 2011; 34: 983–7. doi: 10.1002/jmri.22363 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 131.Messiou C, Collins DJ, Morgan VA, Desouza NM. Optimising diffusion weighted MRI for imaging metastatic and myeloma bone disease and assessing reproducibility. Eur Radiol 2011; 21: 1713–8. doi: 10.1007/s00330-011-2116-4 [DOI] [PubMed] [Google Scholar]
 - 132.Weller A, Papoutsaki MV, Waterton JC, Chiti A, Stroobants S, Kuijer J, et al. Diffusion-weighted (DW) MRI in lung cancers: ADC test-retest repeatability. Eur Radiol 2017; 27: 4552–62. doi: 10.1007/s00330-017-4828-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 133.Blackledge MD, Tunariu N, Orton MR, Padhani AR, Collins DJ, Leach MO, et al. Inter- and intra-observer repeatability of quantitative whole-body, diffusion-weighted imaging (WBDWI) in metastatic bone disease. PLoS One 2016; 11: e0153840. doi: 10.1371/journal.pone.0153840 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 134.Wild JM, Marshall H, Bock M, Schad LR, Jakob PM, Puderbach M, et al. MRI of the lung (1/3): methods. Insights Imaging 2012; 3: 345–53. doi: 10.1007/s13244-012-0176-x [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 135.Biederer J, Beer M, Hirsch W, Wild J, Fabel M, Puderbach M, et al. MRI of the lung (2/3). Why … when … how? Insights Imaging 2012; 3: 355–71. doi: 10.1007/s13244-011-0146-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 136.Biederer J, Mirsadraee S, Beer M, Molinari F, Hintze C, Bauman G, et al. MRI of the lung (3/3)-current applications and future perspectives. Insights Imaging 2012; 3: 373–86. doi: 10.1007/s13244-011-0142-z [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 137.Kumar S, Liney G, Rai R, Holloway L, Moses D, Vinod SK. Magnetic resonance imaging in lung: a review of its potential for radiotherapy. Br J Radiol 2016; 89: 20150431. doi: 10.1259/bjr.20150431 [DOI] [PMC free article] [PubMed] [Google Scholar]
 - 138.Biederer J, Schoene A, Freitag S, Reuter M, Heller M. Simulated pulmonary nodules implanted in a dedicated porcine chest phantom: sensitivity of MR imaging for detection. Radiology 2003; 227: 475–83. doi: 10.1148/radiol.2272020635 [DOI] [PubMed] [Google Scholar]
 - 139.Bergin CJ, Pauly JM, Macovski A. Lung parenchyma: projection reconstruction MR imaging. Radiology 1991; 179: 777–81. doi: 10.1148/radiology.179.3.2027991 [DOI] [PubMed] [Google Scholar]
 







