Published online before print January 9, 2008, 10.1148/radiol.2463062017
(Radiology 2008;246:910-916.)
© RSNA, 2008
Feasibility of Whole-Body MR with T2- and T1-weighted Real-time Steady-State Free Precession Sequences during Continuous Table Movement to Depict Metastases1
Katja Brauck, MD,
Michael O. Zenge, MSc,
Florian M. Vogt, MD,
Harald H. Quick, PhD,
Frank Stock, MSc,
Tanja Trarbach, MD,
Mark E. Ladd, PhD, and
Jörg Barkhausen, MD
1 From the Department of Diagnostic and Interventional Radiology and Neuroradiology (K.B., M.O.Z., F.M.V., H.H.Q., F.S., M.E.L., J.B.) and Department of Internal Medicine, West German Cancer Centre (T.T.), University of Essen, Hufelandstrasse 55, 45122 Essen, Germany. Received November 26, 2006; revision requested January 24, 2007; revision received March 21; accepted April 25; final version accepted September 7.
Address correspondence to J.B. (e-mail: joerg.barkhausen{at}uni-due.de).
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ABSTRACT
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The purpose of the study was to prospectively evaluate a whole-body magnetic resonance (MR) imaging protocol to help depict metastases by using unenhanced T2-weighted and contrast material–enhanced T1-weighted real-time sequences during continuous table movement. The study was conducted after approval of the local institutional review board and written informed consent were obtained. In 11 patients with positron emission tomographic (PET) scans positive for tumors and known metastases, whole-body MR imaging, including T2- and T1-weighted sequences, was performed before and after contrast material administration. A high-precision laser position sensor was used to register the table position for off-line multiplanar reformations of the acquired transverse whole-body data sets. Seventy-three of 75 metastases detected by using PET/computed tomography were correctly diagnosed by using MR imaging. Metastases with a diameter exceeding 5 mm could be visualized in all anatomic regions.
© RSNA, 2008
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INTRODUCTION
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In patients with malignant diseases, therapeutic options, as well as patients' prognoses, strongly depend on the presence of metastases. As metastases may occur in any anatomic region, accurate tumor staging is a prerequisite for therapy planning (1,2). Clinical staging can be time consuming and costly, as it frequently entails several different examinations including conventional radiography, ultrasonography, computed tomography (CT), scintigraphy, and positron emission tomography (PET).
Several studies have shown that magnetic resonance (MR) imaging, combining high spatial resolution and excellent soft-tissue contrast, is superior to other modalities for helping detect and characterize parenchymal and osseous lesions (3–6). However, in general, whole-body MR imaging with surface coils and conventional sequences is time consuming and costly. Therefore, MR is predominantly used to assess individual lesions that cannot be characterized with other modalities.
Recently, advances in imaging technology and the introduction of moving patient platforms with integrated surface coil technology have enabled whole-body MR imaging in a single session. A clinical application has been whole-body MR angiography. The collection of five overlapping three-dimensional data sets allowed coverage of the arterial vessels from head to toe in 72 seconds (7). For whole-body tumor staging, different protocols have been developed by using short tau inversion recovery sequences (8), echo-planar techniques (4), or fast T1-weighted gradient-echo sequences after intravenous contrast material administration (9).
Certain challenges have limited the use of MR in the abdomen and chest. Artifacts caused by involuntary patient movement, insufficient breath holding, or pulsation of the heart can significantly reduce image quality. To overcome these limitations, real-time whole-body imaging during continuous table movement was introduced (10). Motion, which was considered one of the major obstacles in whole-body MR, was used to extend coverage. The major limitation of this approach was the restriction to a single image contrast determined by using T2*/T1 properties of the tissues. Standard steady-state free precession (SSFP) sequences provide good morphologic information and delineate vessels as bright structures, but the accuracy to help detect metastases in parenchymal organs (eg, the liver) is limited (10).
Therefore, the purpose of our study was to prospectively evaluate a whole-body MR imaging protocol to help depict metastases by using unenhanced T2-weighted and contrast material–enhanced T1-weighted real-time sequences during continuous table movement.
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MATERIALS AND METHODS
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Our study was conducted with the approval and in accordance with the regulations of the local institutional review board; written informed consent for this prospective research study was obtained from all subjects prior to the examination. From October 2004 to March 2005, 11 patients (four women, seven men; age range, 39–74 years; mean age, 53 years ± 10 [standard deviation]) were enrolled. Inclusion criteria were PET scans positive for tumors and/or metastases and written informed consent. Of the 11 patients, four had colon carcinoma; two had lung cancer; one patient each had urothelial carcinoma, non-Hodgkin lymphoma, ovarian cancer, and thymic carcinoma; and one patient had a sarcoma in the posterior mediastinum. The whole-body MR examination was performed after the PET/CT examination (mean interval, 10 days ± 6).
MR Examination
Whole-body MR imaging was performed with a 1.5-T system (Magnetom Sonata; Siemens, Erlangen, Germany) with high-performance gradients (maximum amplitude, 40 mT/m; slew rate, 200 mT/m/msec). This imager was equipped with a rolling table platform (BodySURF; MR-Innovation, Essen, Germany), which enabled continuous translation of the patient on a table feed of up to 2000 mm in the bore. Signal reception is accomplished by using two elements of the spine coil, which are integrated into the patient table, and two elements of a multichannel phased-array surface radiofrequency coil. All receiver coils remain stationary in the isocenter during table movement.
The patients were supine and placed feet-first in the imager. The rolling table platform was positioned so that a transverse section in the isocenter of the imager aligned the basal thorax directly cranial to the liver. This position was registered to recenter the patient later during the image protocol. Tuning and shimming were performed only once at this position.
Real-time SSFP sequences were used for all measurements. Although image contrast of standard SSFP images is defined by using the T2/T1 properties of the tissues, this sequence was used to obtain mainly T2-weighted images. To acquire T1-weighted images before and after intravenous administration of 0.2 mmol/kg of contrast material (Magnevist; Schering, Berlin, Germany), a saturation-recovery prepulse was added to the SSFP sequence. The parameters for all real-time sequences were a field of view, 333 x 400 mm; matrix, 256 x 384; and section thickness, 5 mm (Table 1). To achieve continuous three-dimensional data sets without respiratory artifacts, the patients were advised to hold their breath for as long as possible during the thoracic and abdominal images and then to breathe shallowly.
First, T2-weighted images of the entire body were acquired. After repositioning the patient to the starting position, T1-weighted images of the entire body without contrast material were acquired. Prior to contrast material administration, the table was moved so that the section aligned cranial to the liver, as described above. Images of the liver were acquired in the arterial and portal venous phase 20 and 60 seconds after intravenous contrast material administration, respectively. Finally, a T1-weighted whole-body examination was performed (Fig 1).
In all cases, the continuous table translation was performed by an operator (H.Q.) pulling the rolling table platform. To enable multiplanar reformations in any direction for each stack of transverse sections, every image was registered with its table position relative to the isocenter by using a high-precision laser distance sensor (DME 5000; Sick, Waldkirch, Germany) mounted to the wall inside the radiofrequency cabin at the rear of the MR imager. The sensor was controlled by an extra digital signal processing unit, which also calculated the table velocity in real time. The current table velocity relative to a target velocity was provided to the table movement operator on a light-emitting diode display inside the imaging room (11).
The target table velocity for each imaging sequence was determined by using the desired table translation (measured in a longitudinal direction during the acquisition of one section) divided by the acquisition time. Since manual table movement is inherently nonlinear, a section thickness of 5 mm inevitably results in discontinuity artifacts. A table translation of 3.5 mm per section was used in all cases to minimize the discontinuity artifacts, resulting in a target velocity ranging from 15 to 20 mm/sec, depending on the sequence (Table 1).
The position data and table velocity were recorded for every section. At the end of each imaging sequence the average and variance of the table velocity were automatically calculated. A postprocessing routine inserted the position data in the Digital Imaging and Communications in Medicine header information. Data reformatting was performed on a three-dimensional image processing workstation (Advantage Workstation 4.0; GE Medical Systems, Barrington, Ill) by a radiologist (K.B., with 2 years experience). Continuous moving table whole-body MR imaging was successfully performed in all patients.
PET/CT Examination
PET/CT imaging was performed with a scanner (Biograph; Siemens Medical Solutions, Hoffman Estates, Ill). Whole-body CT (130 mAs, 130 kV, 5-mm sections, 8-mm table feed, and 2.4-mm incremental reconstruction) covered a region from the skull base to the upper thighs after intravenous administration of 140 mL of iodinated contrast agent (Xenetix 300; Guerbet, Sulzbach, Germany). A limited breath-hold technique was used to avoid motion-induced artifacts in the area of the diaphragm (12).
PET images were acquired 60 minutes after the administration of fluorine 18 fluorodeoxyglucose (300–340 MBq, adapted to body weight), covering the same field of view as with CT. Images were corrected for scatter and were iteratively reconstructed. Before the injection of the radioactive tracer, a blood sample was taken to ensure blood glucose levels were normal.
Image Analysis
PET/CT data sets of all 11 patients were analyzed in consensus by an experienced nuclear medicine physician and a radiologist (both nonauthors, with 5 and 12 years experience, respectively). They had access to patient information including age, sex, primary tumor, tumor stage, and previous imaging tests. The diagnosis of metastasis was made on the basis of morphologic criteria and/or a standard uptake value of more than 3.5 for liver lesions and more than 2.5 for all other lesions. Metastases with a diameter of less than 5 mm were excluded from the evaluation; for all other metastases, the location and maximum diameter were recorded.
Immediately after the MR imaging, a clinical reading was performed by an author (K.B., with 3 years experience) to decide whether additional examinations (dedicated MR imaging) are required to make a final diagnosis. Thereafter, the study reading (evaluation and assessment of image quality) was performed in consensus by two radiologists (F.V., J.B., with 5 and 8 years experience, respectively). To minimize recall bias, the time between the image readings from different MR sequences was at least 4 weeks. The readers had access to patient information including age, sex, and primary tumor, but they were blinded to the results of the PET/CT examinations and all other imaging procedures performed prior to the whole-body MR and additional MR imaging. The images from the different MR sequences, including sagittal and coronal reformations, were read separately, in random order, in three different sessions, followed by a fourth session for a combined reading of images from all three sequences.
Overall image quality, as well as the presence of motion artifacts resulting from continuous table movement, was assessed on a five-point scale, where a score of 1 = nondiagnostic (anatomic regions of interest unassessable, severe motion artifacts), a score of 2 = poor (anatomic regions of interest barely assessable, obvious motion artifacts), a score of 3 = fair (anatomic regions of interest incompletely assessable, fewer motion artifacts), a score of 4 = good (anatomic regions of interest assessable, minimal motion artifacts), and a score of 5 = excellent (anatomic regions of interest are assessable, no motion artifacts). The presence of metastases within lymph nodes, lung, liver, and bones was recorded for the different real-time sequences. Finally, a combined reading of images from all MR sequences was performed.
Liver, lung, and bone metastases were suspected in the case of focal lesions with signal intensities different from those of the surrounding tissues, whereas the diagnosis of lymph node metastasis was made on the basis of size, as well as increased signal intensities on T2-weighted images and/or an increased contrast enhancement. If the real-time MR image helped detect additional metastases when compared with the PET/CT examination, a dedicated contrast-enhanced MR imaging of the region was performed.
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RESULTS
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The calculated average table velocity did not exceed the requested table velocity by more than 5.6 mm/sec in any of the moving table MR examinations, while the maximum variance in each measurement was not larger than 5.7 mm/sec. The position feedback permitted sagittal and coronal reformations and confirms our concept by using a sensor to register table position for continuous acquired data sets (Fig 2).
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Figure 2a: Transverse T1-weighted images in 55-year-old man with multiple liver metastases (arrows) from colon cancer. (a, b) Images without contrast agent (2.08/1.04; flip angle, 50°, acquisition time, 221 msec; scan time, 115 seconds) and (c, d) after contrast agent administration (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 27 seconds). Note coronal reformations of real-time sequences (b, d).
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Figure 2b: Transverse T1-weighted images in 55-year-old man with multiple liver metastases (arrows) from colon cancer. (a, b) Images without contrast agent (2.08/1.04; flip angle, 50°, acquisition time, 221 msec; scan time, 115 seconds) and (c, d) after contrast agent administration (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 27 seconds). Note coronal reformations of real-time sequences (b, d).
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Figure 2c: Transverse T1-weighted images in 55-year-old man with multiple liver metastases (arrows) from colon cancer. (a, b) Images without contrast agent (2.08/1.04; flip angle, 50°, acquisition time, 221 msec; scan time, 115 seconds) and (c, d) after contrast agent administration (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 27 seconds). Note coronal reformations of real-time sequences (b, d).
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Figure 2d: Transverse T1-weighted images in 55-year-old man with multiple liver metastases (arrows) from colon cancer. (a, b) Images without contrast agent (2.08/1.04; flip angle, 50°, acquisition time, 221 msec; scan time, 115 seconds) and (c, d) after contrast agent administration (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 27 seconds). Note coronal reformations of real-time sequences (b, d).
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Image Quality
Continuous table movement did not result in artifacts that hampered the evaluation of the transverse images. However, owing to tuning and shimming only at a single location, slight differences of the image contrast and off-resonance artifacts in the subcutaneous fat and the tissue-air interface could be detected. The mean score of the image quality was 3.7 for T2, 2.9 for T1 without intravenous contrast agent and 3.9 for the contrast-enhanced T1-weighted sequences.
Metastases
PET/CT helped detect 75 metastases with a diameter of more than 5 mm in our study cohort. Of those, there were 28 lymph node metastases (mean diameter, 2.3 cm ± 2.5; range, 1.1–7.7 cm) (Fig 3), 27 liver metastases (mean diameter, 2.7 cm ± 1.5; range, 0.8–7.1 cm), 13 pulmonary metastases (mean diameter, 2.3 cm ± 1.6; range, 0.6–8.1 cm), and seven were bone metastases (mean diameter, 2.2 cm ± 0.7; range, 1.7–3.5 cm).
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Figure 3a: Transverse pelvic MR images in 62-year-old male with non-Hodgkin lymphoma and enlarged inguinal lymph nodes (arrows): (a) T2-weighted (2.34/1.17; flip angle, 55°; acquisition time per image, 175 msec; scan time, 91.1 seconds), (b) T1-weighted without contrast material (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 115 seconds); (c) contrast-enhanced T1-weighted (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 115 seconds), and (d) fused PET/CT images.
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Figure 3b: Transverse pelvic MR images in 62-year-old male with non-Hodgkin lymphoma and enlarged inguinal lymph nodes (arrows): (a) T2-weighted (2.34/1.17; flip angle, 55°; acquisition time per image, 175 msec; scan time, 91.1 seconds), (b) T1-weighted without contrast material (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 115 seconds); (c) contrast-enhanced T1-weighted (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 115 seconds), and (d) fused PET/CT images.
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Figure 3c: Transverse pelvic MR images in 62-year-old male with non-Hodgkin lymphoma and enlarged inguinal lymph nodes (arrows): (a) T2-weighted (2.34/1.17; flip angle, 55°; acquisition time per image, 175 msec; scan time, 91.1 seconds), (b) T1-weighted without contrast material (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 115 seconds); (c) contrast-enhanced T1-weighted (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 115 seconds), and (d) fused PET/CT images.
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Figure 3d: Transverse pelvic MR images in 62-year-old male with non-Hodgkin lymphoma and enlarged inguinal lymph nodes (arrows): (a) T2-weighted (2.34/1.17; flip angle, 55°; acquisition time per image, 175 msec; scan time, 91.1 seconds), (b) T1-weighted without contrast material (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 115 seconds); (c) contrast-enhanced T1-weighted (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 115 seconds), and (d) fused PET/CT images.
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In total, 73 of 75 total metastases and 26 of 28 lymph node metastases were detected by using MR imaging (Fig 3); two abdominal lymph node metastases were missed owing to overlaying bowel. In the lung parenchyma, real-time MR imaging detected all 13 metastases. All liver metastases exceeding a diameter of 5 mm detected by using PET/CT were correctly diagnosed by using MR. In the skeletal system, all seven metastatic lesions detected by using PET/CT were also seen on the real-time MR images. However, real-time MR detected seven additional bone lesions in the spine (Fig 4), which were confirmed by additional dedicated contrast-enhanced MR examinations.
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Figure 4a: Transverse MR images in 62-year-old male with non-Hodgkin lymphoma with additional bone metastases (arrow) in thoracic spine not seen at PET/CT. (a, b) Contrast-enhanced T1-weighted images (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 115 seconds) and (c, d) fused PET/CT images in the same position.
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Figure 4b: Transverse MR images in 62-year-old male with non-Hodgkin lymphoma with additional bone metastases (arrow) in thoracic spine not seen at PET/CT. (a, b) Contrast-enhanced T1-weighted images (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 115 seconds) and (c, d) fused PET/CT images in the same position.
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Figure 4c: Transverse MR images in 62-year-old male with non-Hodgkin lymphoma with additional bone metastases (arrow) in thoracic spine not seen at PET/CT. (a, b) Contrast-enhanced T1-weighted images (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 115 seconds) and (c, d) fused PET/CT images in the same position.
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Figure 4d: Transverse MR images in 62-year-old male with non-Hodgkin lymphoma with additional bone metastases (arrow) in thoracic spine not seen at PET/CT. (a, b) Contrast-enhanced T1-weighted images (2.08/1.04; flip angle, 50°; acquisition time per image, 221 msec; scan time, 115 seconds) and (c, d) fused PET/CT images in the same position.
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Comparison between the Different Sequences of the Whole-Body MR Examinations
The three real-time sequences to help detect metastases used in our study delivered different results (Table 2). The most metastases were detected with the T1-weighted SSFP images after contrast material administration (Fig 2), whereas the unenhanced T1-weighted SSFP sequences had the lowest detection rate. However, the T2-weighted SSFP sequences helped detect more pulmonary lesions than did the T1-weighted sequences by using intravenous contrast material. Thus, the combined reading of images from all three sequences yielded the highest detection rate.
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DISCUSSION
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Almost a decade ago, Johnson et al (13) introduced an echo-planar imaging technique that acquired a stack of 180 transverse images in 18 seconds. The initial results were encouraging and the majority of metastases could be detected. Similar results are reported by Horvath et al (4) who imaged patients with breast cancer from head to toe with the same technique. In comparison with conventional staging techniques, whole-body echo-planar imaging was more accurate. The fast data acquisition capabilities of echo-planar imaging results in imaging times comparable with state-of-the-art multisection CT, but the technique had several limitations. The whole-body protocol provided heavily T2-weighted images only, and image quality suffered from susceptibility artifacts inherent to echo-planar imaging. Additionally, time-consuming shimming or tuning for transmitter and receiver adjustment had to be performed to ensure sufficient image quality.
Walker et al (3) introduced whole-body turbo short inversion time inversion recovery sequences for the evaluation of metastases. Four overlapping stacks of coronal images were collected with an average imaging time of 20 minutes. The results were superior to those obtained with conventional imaging including radiography, CT, scintigraphy, and PET, especially for osseous lesions. These promising findings were confirmed by additional studies (14,15). However, the long imaging time and poor presentation of thoracic lesions, owing to respiratory and cardiac motion artifacts, were important disadvantages.
The introduction of real-time SSFP sequences combining fast data acquisition capabilities with a reproducible image quality overcame several limitations of the earlier techniques (10). More than 300 transverse sections could be collected in 30 seconds without time-consuming shimming or adjustments. However, this approach had two major limitations. First, the SSFP sequences provided an image contrast defined by the T2/T1 properties of tissues, which is far from being perfect for helping detect metastases. Additionally, all data were collected in the isocenter without any information about z-position, ruling out multiplanar reformations.
The technique used in our study overcomes these limitations and combines most of the postulated requirements for whole-body MR imaging in cancer patients. Imaging from head to toe can be performed by using overlapping 5-mm sections and reasonable in-plane resolution in less than 10 minutes without time-consuming shimming or transmitter adjustments. Additionally, the fast data acquisition capabilities of SSFP sequences allow for real-time imaging without cardiac or respiratory motion artifacts. The standard and saturation-recovery SSFP sequences combined with intravenous contrast material administration provide different image contrasts.
The introduced protocol with or without contrast material yields advantages when compared with other protocols that used only contrast-enhanced T1-weighted or T2-weighted images. Comparing the three sequences, the T1-weighted sequences after contrast material administration yielded the highest detection rate. However, the combination of mainly T2-weighted and contrast-enhanced T1-weighted images further increased the number of lesions and led to the detection of 73 of 75 metastases with a diameter exceeding 5 mm.
The position registration of a stack of transverse sections enabled multiplanar reformations of the data sets. Although manual table movement resulted in nonlinear table movement, the acquisition of overlapping transverse sections allowed sagittal and coronal reconstructions, which can be used to receive additional information. The applied section thickness of 5 mm proved to be an adequate compromise between signal-to-noise ratio and through-plane resolution. However, the limited resolution in the z-direction owing to signal-to-noise ratio restrictions must be considered as an important drawback of two-dimensional imaging. Therefore, automatic, continuously moving table three-dimensional data acquisition techniques, as they have recently become available by some manufacturers, may simplify our protocol and may be an attractive alternative (11,16).
Our study had several limitations. The spatial resolution of our MR technique is much lower compared with that of PET/CT. However, the high soft-tissue contrast inherent in MR imaging might partially compensate for that. Additionally, tuning and shimming was performed only at a single location prior to data acquisition. This can lead to contrast variations and off-resonance artifacts. Moreover, SSFP sequences only provide mainly T2-weighted images. The T1 contrast depends on the application of a saturation-recovery pulse (17). This technique has been reported primarily for the assessment of myocardial perfusion (18,19). The diagnostic accuracy of these sequences has to be compared with conventional T2- and T1-weighted images in a larger patient cohort. Furthermore, studying only patients with abnormal PET findings biases the data. The small number of patients must also be considered another limitation of our study, because a recall bias cannot completely be avoided. However, our study clearly demonstrates the feasibility of multiple contrast-enhanced real-time whole-body MR examinations, and we hope that these data encourage others to participate in larger multicenter trials to evaluate the diagnostic potential of this new technique.
In conclusion, it is feasible to use whole-body MR imaging to help depict metastases by using T1- and T2-weighted real-time SSFP sequences. More than 800 transverse real-time images combining insensitivity to motion artifacts and sufficient spatial resolution can be collected in less than 10 minutes. Of 75 metastases exceeding a diameter of 5 mm detected with PET/CT, 73 were detected with MR. However, diagnostic accuracy has to be determined in larger clinical studies.
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ADVANCE IN KNOWLEDGE
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- Whole-body MR imaging with real-time transverse T2- and T1-weighted steady-state free precession sequences to help depict metastases is feasible and aided in the diagnosis of 73 of 75 metastases that were also depicted with PET/CT.
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IMPLICATION FOR PATIENT CARE
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- Whole-body multicontrast real-time MR is feasible to help depict metastases; however, larger studies are needed.
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FOOTNOTES
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Abbreviations: SSFP = steady-state free precession
Author contributions: Guarantor of integrity of entire study, J.B.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, M.E.L.; clinical studies, K.B., F.M.V., T.T., J.B.; experimental studies, M.O.Z., H.H.Q., F.S., M.E.L.; and manuscript editing, K.B., M.O.Z., H.H.Q., M.E.L., J.B.
Authors stated no financial relationship to disclose.
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ABSTRACT
INTRODUCTION
