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AJR 2002; 179:445-449
© American Roentgen Ray Society


Original Report

Three-Dimensional Volumetric Interpolated Breath-Hold MR Imaging for Whole-Body Tumor Staging in Less Than 15 Minutes: A Feasibility Study

Thomas C. Lauenstein1, Susanne C. Goehde1, Christoph U. Herborn1, Wiebke Treder2, Stefan G. Ruehm1, Jörg F. Debatin1 and Jörg Barkhausen1

1 Department of Diagnostic Radiology, University Hospital Essen, Hufelandstr. 55, D-45122 Essen, Germany.
2 Department of Internal Medicine and Cancer Research, University Hospital Essen, D-45122 Essen, Germany.

Received October 17, 2001; accepted after revision February 11, 2002.

 
Address correspondence J. Barkhausen.


Abstract
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. The purpose of our study was to evaluate the feasibility and accuracy of three-dimensional (3D) volumetric interpolated breath-hold whole-body MR imaging using CT and nuclear medicine techniques as the standard of reference in patients with metastases.

CONCLUSION. The 3D volumetric interpolated breath-hold whole-body MR imaging examination for metastases screening correlates well with CT and scintigraphy. The use of the rolling table platform permits rapid whole-body imaging in an average of 11 min. The preliminary results indicate that the described technique has the potential to emerge as an all-encompassing alternative to conventional multimodality tumor staging strategies.


Introduction
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Many primary tumors including those originating in the breast, lung, colon, or testis are frequently associated with metastases even at the time of the patient's first presentation. More than any other factor, the presence of metastases affects subsequent therapeutic options and hence patient prognosis. Because metastatic disease can affect any anatomic region, staging strategies are designed to cover the entire body and generally encompass multiple examinations including conventional radiography, sonography, CT, MR imaging, scintigraphy, and, recently, positron emission tomography. The precise combination of imaging modality and anatomic region is tailored to the primary cancer under consideration [1, 2]. Independent of their particular design, staging examinations are time-consuming and costly. Despite all efforts, the diagnostic accuracy of staging examinations remains limited in many cases. To monitor the effect of therapies, operators need to perform repeated staging examinations at regular intervals, which can result in considerable exposure of ionizing radiation to the patient [3], especially in young patients with good prognoses who require regular CT.

On the basis of the potential to overcome some of the outlined limitations, whole-body MR imaging has been evaluated for the detection of bone metastases [4, 5] and has been proposed for generalized tumor staging [6, 7]. Limitations of this compelling whole-body MR imaging concept have included long examination times exceeding 40 min [4] in combination with limited spatial resolution and the presence of imaging artifacts [6].

Recently, the volumetric interpolated breath-hold examination, a fat-saturated three-dimensional (3D) gradient-echo sequence with nearly isotropic resolution, has become available [8]. Although preserving adequate anatomic coverage and uniform fat saturation, the volumetric interpolated breath-hold 3D data sets are collected within the confines of a single breath-hold. In the abdomen, the volumetric interpolated breath-hold examination has been shown to provide image quality comparable with that of conventional fat-saturated two-dimensional gradient-echo images [9]. Inherently low signal-to-noise ratio requires the use of surface coils for signal reception. Extending the volumetric interpolated breath-hold high-resolution coverage from single to multiple anatomic regions toward a whole-body examination mandates rapid patient movement in conjunction with surface coil—based data reception. These requirements are fulfilled by a rolling table platform with integrated surface coils developed for whole-body MR angiography (AngioSURF system for unlimited rolling field of view; MR Innovation, Essen, Germany) [10]. The technique was adapted for the purpose of whole-body MR imaging.

The purpose of this study was to evaluate the feasibility and accuracy of a volumetric interpolated breath-hold examination in conjunction with the AngioSURF platform for whole-body MR imaging using CT and nuclear medicine techniques as the standard of reference in patients with metastases.


Materials and Methods
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
From July 2001 to August 2001, four female patients with breast cancer (age range, 39-63 years; mean age, 52.3 years) and four male patients with testicular cancer (age range, 21-36 years; mean age, 29.0 years) were included in this study, which was conducted in accordance with all guidelines set forth by the approving institutional review board. Informed consent was obtained before each examination. Exclusion criteria were based on contraindications to MR imaging, including the presence of a pacemaker, metallic implants in critical organs, severe claustrophobia, and a lack of willingness or ability to sign the informed consent.

MR Imaging
MR examinations were performed on a 1.5-T system (Magnetom Sonata; Siemens Medical Systems, Erlangen, Germany) equipped with high-performance gradient systems characterized by a maximal gradient amplitude of 40 mT/m and a slew rate of 200 mT/m/msec. The volumetric interpolated breath-hold examination is based on a 3D spoiled gradient-echo acquisition. The sequence parameters include a TR/TE of 3.1/1.2 msec, a flip angle of 12°, and a bandwidth of 490 Hz/pixel. A slab thickness of 312 mm was used for all measurements. Sixty-five partitions were obtained that were subsequently interpolated to 104 partitions resulting in a final slice thickness of 3 mm. A rectangular (5/8) field of view of 350 x 219 mm2 and a data acquisition matrix of 120 x 256 data points resulted in an in-plane resolution of 1.8 x 1.4 mm2, which was interpolated by zero filling to a matrix of 240 x 512 for a final pixel size of 0.9 x 0.7 mm2. As a result of partial Fourier in both the ky (7/8) and kz (6/8) phase-encoding directions, the data-acquisition time of a 3D volume was 22 sec. The 3D sequence incorporates a frequency-selective fat-saturation pulse before each partition loop, which is centrically recorded to maximize fat saturation.

Patients were placed in the supine position on the rolling table platform (Fig. 1), which is mounted on the original patient table of any MR imaging system (Symphony or Vision; Siemens Medical Systems). For easy movement in the z direction, the rolling table platform (length, 270 cm; width, 33-50 cm) is placed on seven pairs of roller bearings that are easily installed on the patient table. Signal reception is accomplished using two elements of the spine coil, which are integrated into the patient table, and the body phased array coil, which remains stationary by being attached to the original patient table. The rolling table platform glides the patient over the stationary patient table through the isocenter of the magnet between the posteriorly located spine coils and the anteriorly located body phased array coil.



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Fig. 1. Photograph shows patient in supine position on rolling table platform capable of pulling patient through magnet bore and phased array surface coil. Rolling table platform is mounted on original patient table. Signal reception uses two elements of spine coil, which are integrated into patient table, and body phased array coil, which remains stationary, attached to patient table in bore.

 

A coronal localizer sequence of the upper abdomen that encompassed the entire liver was acquired. From this basis, further landmarks were defined in 26-cm steps in the cranial direction for imaging the thorax and skull and in the caudal direction for imaging the pelvis, femur, and knee region. All 3D data sets were collected in the axial plane, resulting in a craniocaudal coverage of 31.2 cm. To compensate for possible wrap around artifacts at the border of each 3D data set, we overlapped the acquisitions by 2.6 cm.

Paramagnetic contrast material (gadopentetate dimeglumine, Magnevist; Schering, Berlin, Germany) was applied IV into the antecubital vein using an automatic injector (Spectris; Medrad, Germany). Injection parameters included a dose of 0.2 mmol/kg gadopentetate dimeglumine and a flow rate of 3 mL/sec followed by rapid injection of 20 mL of normal saline at the same flow rate. Depending on body height, patients were examined in seven (n = 5) or eight steps (n = 3). After a delay of 20 and 60 sec after contrast administration, the first two 3D data sets of the abdomen, encompassing the entire liver, were performed in the axial plane with patients breath-holding. Subsequently, the rolling table platform was moved manually to the chest region, where a coronal 3D data set was collected. The 8 sec required to move the platform was used to provide breathing instructions. Subsequently, the platform was moved to permit the acquisition of axial 3D data sets of the pelvis, the femur or knee, and the skull. Finally, the platform was moved back to the abdomen, where a third abdominal data set was collected. The entire imaging time was 3 min 52 sec for the seven-step protocol and 4 min 22 sec for the eight-step protocol.

Reference Examinations
All patients underwent thoracic, abdominal, and pelvic helical CT. In three patients, contrast-enhanced helical CT was performed to exclude brain metastases. Furthermore, five patients underwent skeletal scintigraphy. All examinations were performed 3-13 days (average, 7.6 days) before the whole-body MR examination.

Data Analysis
The 3D MR imaging data sets of each whole-body examination were analyzed interactively by two radiologists on a workstation (Virtuoso; Siemens Medical Systems) in the multiplanar reformation mode. Discrepancies were resolved by consensus. Reviewers did not have information about the results of other imaging modalities. Information about patient age, sex, and primary tumor were provided. Images were evaluated for the presence of metastatic disease. Metastases were numerically quantified for lung; liver; bones; and other anatomic regions including the cerebrum, retroperitoneum, and skin. The diameter of the smallest metastasis detected on whole-body MR imaging for each anatomic region was measured. Whole-body MR findings were directly compared with the reference examinations to evaluate agreement.


Results
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Whole-body MR imaging was possible in all eight patients. There were no complications regarding the handling of the rolling table platform. The mean room time was 11 ± 2 min including data acquisition time of approximately 4 min for the 3D sequences of the different anatomic regions.

Whole-body MR imaging detected hepatic metastases in six patients (Fig. 2A,2B). In three patients, more than five hepatic metastases were identified. The smallest hepatic metastasis measured 6 mm in diameter. No false-negative findings were revealed on MR imaging. Whole-body MR imaging detected pulmonary metastases in five patients. In one patient, a lung metastasis measuring 5 mm in diameter on CT was missed on MR imaging. The smallest pulmonary metastasis measured 8 mm in diameter (Fig. 3A,3B). In addition, MR imaging revealed retroperitoneal metastases in one patient with testicular cancer and a metastases in the dorsal abdominal wall in another patient. Both findings were confirmed on CT.



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Fig. 2A. 39-year-old woman with breast cancer. Whole-body MR image of liver shows hepatic metastasis (arrow).

 


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Fig. 2B. 39-year-old woman with breast cancer. Axial contrast-enhanced CT scan confirms presence of hepatic metastasis (arrow) shown in A.

 


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Fig. 3A. 54-year-old woman with breast cancer. Whole-body MR image of lungs shows pulmonary metastases (arrows).

 


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Fig. 3B. 54-year-old woman with breast cancer. Axial contrast-enhanced CT scan confirms presence of pulmonary metastases (arrows) shown in A.

 

Bone metastases evidenced by increased signal intensity on contrast-enhanced volumetric interpolated breath-hold images were detected on MR imaging in four patients. Locations included the spine (n = 3), pelvis (n = 3), and ribs (n = 2). Furthermore, in two patients, osseous metastases were seen in the scapula and the femur. Bone scintigraphy, used as the standard of reference, revealed good correlation with MR imaging (Fig. 4A,4B,4C) except in one patient. In this patient, MR imaging had revealed osseous lesions in the lumbar spine, whereas skeletal scintigraphy did not. Eventually, the presence of bone metastasis was confirmed at biopsy. All other MR imaging findings regarding osseous metastases were confirmed on skeletal scintigraphy.



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Fig. 4A. 53-year-old woman with breast cancer and osseous metastases. Coronal reformatted whole-body MR image of pelvis shows osseous metastases (arrows).

 


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Fig. 4B. 53-year-old woman with breast cancer and osseous metastases. Whole-body MR image of thorax shows bone metastasis in right rib (arrow).

 


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Fig. 4C. 53-year-old woman with breast cancer and osseous metastases. Skeletal scintigram confirms presence of bone metastases (arrows) shown in A and B.

 

Cerebral metastases ranging between 8 and 15 mm in diameter were detected on MR imaging in two patients. All metastases, and their absence in a third patient, were confirmed on CT (Fig. 5A,5B).



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Fig. 5A. 36-year-old man with testicular carcinoma. Oblique reformatted MR image shows 10-mm cerebral metastasis (arrow).

 


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Fig. 5B. 36-year-old man with testicular carcinoma. Contrast-enhanced CT scan of brain confirms cerebral metastasis (arrow) shown in A.

 


Discussion
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
The preliminary results of the described technique indicate that 3D whole-body MR imaging has the potential to emerge as an all-encompassing alternative to conventional multimodality tumor staging strategies. The rolling table platform with an integrated surface coil enables the acquisition in rapid succession of high-resolution 3D MR image sets covering all anatomic regions from the skull to the tibia. Beyond whole-body coverage, the technique even permits dynamic imaging of parenchymal organs in the abdomen. The short examination is non-invasive, is not associated with radiation exposure, and does not rely on nephrotoxic contrast material. Data from eight patients revealed excellent correlation with standard staging examinations including CT and bone scintigraphy.

The concept of whole-body MR imaging is not new [4,5,6,7]. Long scanning times and poor image quality characterized by extensive artifacts have limited its clinical impact [4, 6, 7]. In conjunction with a fat-saturated ultrafast 3D gradient-echo sequence, the application of the rolling table platform overcomes some of these limitations. After being placed on the platform, the patient is moved through the MR scanner and through an integrated coil sandwich without a new landmark being acquired for each step of the whole-body examination. Hence, high image quality can be obtained throughout all stations, and even small lesions are readily detected and distinguished from surrounding tissues.

Most whole-body MR imaging concepts are based on echoplanar sequence designs [6, 11]. Johnson et al. [11] presented a technique on the basis of the acquisition of a stack of transverse T2-weighted echoplanar images, using the body coil for both signal transmission and reception. An automatic table moved the patient through the gantry. The results were encouraging because most abnormalities could be detected. Horvath et al. [6] reported similar results for whole-body echoplanar MR imaging of patients with breast cancer, which rendered correct findings in 95% of patients. Apparent limitations of the technique included a low signal-to-noise ratio resulting in reduced spatial resolution and magnetic susceptibility effects amplified by inconsistent shimming over the different body regions, causing considerable distortions in echoplanar image contrast and geometry. A recent study assessing true fast imaging with steady-state precession for whole-body MR imaging documented poor image contrast and low spatial resolution as significant limitations [7].

The whole-body MR examination overcomes these limitations. The three-dimensional volumetric interpolated breath-hold data sets provide high-resolution images with nearly isotropic voxels. In conjunction with zero-filling routines, the voxel dimensions could be reduced to 0.7 x 0.9 x 3.0 mm. The sequence is T1-weighted, thus documenting the enhancement of paramagnetic contrast material. In conjunction with fat saturation, areas characterized by increased contrast material uptake in the parenchymal organs and the skeletal system are easily detected. Fast imaging routines permit the collection of a first abdominal data set in the arterial phase followed by a second data set obtained in the portal venous phase. A delayed 3D data set completes the assessment of the liver. This type of dynamic 3D imaging has been documented to be most accurate in the detection and characterization of hepatic mass lesions [12]. Thus, all hepatic metastases documented on multiphase dynamic CT were also seen on whole-body 3D volumetric interpolated breath-hold MR imaging.

Outside the abdomen, the 3D data is collected in the equilibrium phase. The enhancement characteristics in this late phase are well suited for the detection of cerebral and osseous lesions. In this limited study, the MR 3D data sets proved sufficient for visualization of all cerebral and osseous metastases identified on CT and bone scintigraphy, respectively. In fact, whole-body MR imaging revealed one-bone metastases not detected on skeletal scintigraphy and later confirmed at biopsy. Limitations of skeletal scintigraphy are well known, as is the fact that MR imaging is more sensitive in the detection of metastases from some primary tumors [4]. Limitations inherent to the 3D volumetric interpolated breath-hold concept seemed evident in the lungs. Although only a single 5-mm lesion was missed, the underlying image quality compared poorly with CT scanning. Perhaps the incorporation of other sequences such as half-Fourier acquired single-shot turbo spin echo could have improved assessment of the lungs for metastatic disease.

The examination time is minimized by obviating patient and coil repositioning. The rolling table concept, which has been successfully applied to whole-body MR angiography [10], provides extended craniocaudal coverage in 1 min 12 sec. The short overall examination time of less than 15 min contributes to high patient acceptance. More important, from a diagnostic perspective, the time required to collect the 3D data sets after the contrast injection amounts to 4 min. During this time interval, sufficient paramagnetic contrast material will remain in the lesions to permit their ready identification.

Certainly, whole-body MR imaging will not replace dedicated MR examinations, which can exploit a host of different contrast mechanisms for the study of individual organ systems. The aim of the described strategy is focused solely on the detection and follow-up of metastatic lesions in patients with known primary tumors. If identified lesions cannot be reliably characterized as metastatic, additional examinations are required. Naturally, the clinical potential of whole-body MR imaging should be evaluated on the basis of larger patient cohorts—we are hopeful that this first report will motivate others to help in this regard.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

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  9. Lee VS, Lavelle MT, Rofsky NM, et al. Hepatic MR imaging with a dynamic contrast-enhanced isotropic volumetric interpolated breath-hold examination: feasibility, reproducibility, and technical quality. Radiology 2000;215:365 -372[Abstract/Free Full Text]
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