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DOI: 10.1148/radiol.2392050411
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(Radiology 2006;239:481-487.)
© RSNA, 2006

Genitourinary Imaging

Prostate Cancer Evaluated with Ferumoxtran-10–enhanced T2*-weighted MR Imaging at 1.5 and 3.0 T: Early Experience1

Roel A. M. Heesakkers, MD, Jurgen J. Fütterer, MD, PhD, Anke M. Hövels, MSc, Harrie C. M. van den Bosch, MD, Tom W. J. Scheenen, PhD, Yvonne L. Hoogeveen, PhD and Jelle O. Barentsz, MD, PhD

1 From the Departments of Radiology (R.A.M.H., J.J.F., T.W.J.S., Y.L.H., J.O.B.) and Medical Technology Assessment (A.M.H.), University Medical Center Nijmegen, Geert Grooteplein zuid 10, NL 6500 HB, Nijmegen, the Netherlands; and Department of Radiology, Catharina Hospital, Eindhoven, the Netherlands (H.C.M.v.d.B.). From the 2004 RSNA Annual Meeting. Received March 11, 2005; revision requested May 3; revision received May 26; accepted June 21; final version accepted August 1. Supported by ZonMw The Netherlands Organization for Health Research and Development. Address correspondence to R.A.M.H. (e-mail: r.heesakkers{at}rad.umcn.nl).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Purpose: To prospectively evaluate the feasibility of ferumoxtran-10–enhanced magnetic resonance (MR) imaging at high magnetic field strength (3.0 T) and to compare image quality between 1.5- and 3.0-T MR imaging in terms of lymph node detection in patients with prostate cancer.

Materials and Methods: This study was institutional review board approved, and all patients gave written informed consent. Forty-eight consecutive patients aged 51–79 years (mean, 65.5 years) with prostate cancer were enrolled. T2*-weighted 1.5- and 3.0-T MR images of the pelvis were acquired in a sagittal plane parallel to the psoas muscle 24 hours after ferumoxtran-10 administration. A pelvic and body phased-array coil was used and yielded an in-plane resolution of 0.56 x 0.56 x 3.00 mm at 1.5 T and 0.50 x 0.50 x 2.50 mm at 3.0 T. All images were evaluated by three readers for total image quality, lymph node border delineation, muscle-fat contrast, and vessel-fat contrast. Statistical significance was calculated by using the Mann-Whitney U test. Subsequently, the general linear mixed model was used to estimate the contributions of three factors—patient, reader, and technique—to the variability of the imaging results.

Results: Significantly (P < .05) better muscle-fat contrast, vessel-fat contrast, lymph node border delineation, and total image quality were observed at 3.0-T MR imaging. The general linear mixed model revealed that the variability of all results could be attributed to the use of 3.0-T imaging.

Conclusion: Ferumoxtran-10–enhanced MR imaging can be performed at high magnetic field strengths and result in improved image quality, which may lead to improved detection of small positive lymph nodes.

© RSNA, 2006


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Prostate cancer is one of the most common malignancies in men (1). Pelvic lymph nodes have an important role in indicating whether the prostate carcinoma is curable. A detected lymph node that harbors metastasis is called a positive lymph node. One positive lymph node can prompt a change in the classification of prostate cancer from local disease to systemic disease that is resistant to curative treatment (2,3). Harisinghani et al (4) reported that performing magnetic resonance (MR) imaging enhanced with ultrasmall particles of the iron oxide ferumoxtran-10 significantly improved the detection of metastases in normal sized lymph nodes. These iron particles accumulate in normal lymph node tissue within 24–36 hours after they are intravenously injected (5). With ferumoxtran-10–enhanced MR imaging, one can take advantage of the susceptibility difference created by the iron particles. Owing to this effect, all normal lymph nodes appear black (ie, with low signal intensity) on T2*-weighted images. Metastatic nodes remain unchanged, usually maintaining high signal intensity, on T2*-weighted images because of the lack of iron particles in metastatic tissue. With ferumoxtran-10–enhanced MR imaging, 5–10-mm-diameter positive lymph nodes can be detected with standard clinical 1.5-T MR imaging units (4,6). In comparison, the smallest metastatic pelvic nodes that can be detected with positron emission tomography (PET) are 6–10 mm in diameter (7). Metastatic depositions smaller than 5 mm can be detected with ferumoxtran-10–enhanced MR imaging but not reliably (4).

Clinical 3.0-T whole-body MR systems are increasingly becoming available. The use of such a high magnetic field strength, owing to the resulting higher signal-to-noise ratio, is expected to enable imaging with a higher spatial resolution. One could therefore expect smaller positive nodes to be detected with use of ferumoxtran-10–enhanced 3.0-T MR imaging. In brain MR imaging, the use of higher magnetic field strengths has resulted in an increase in the signal-to-noise ratio (8,9); however, it has also yielded shorter T2 relaxation times and longer T1 relaxation times (10). Other differences with 3.0-T imaging are increased susceptibility artifact, specific absorption rate, and homogeneity problems. Because peristalsis is inevitable and the MR sequences are too long for breath-holding techniques to be used, images of the pelvic nodes may be degraded. Furthermore, ferumoxtran-10 uses the T1 and T2* susceptibility effects of the iron oxide, which are shorter at 3.0 T. Thus, the question arises: Is ferumoxtran-10–enhanced MR imaging performed at higher magnetic field strengths feasible and is it improved by a higher signal-to-noise ratio, or will increased artifacts degrade lymph node evaluation?

Thus, the purpose of our study was to prospectively evaluate the feasibility of ferumoxtran-10–enhanced MR imaging at high field strength (3.0 T) and to compare image quality between 1.5- and 3.0-T MR imaging in terms of lymph node detection in patients with prostate cancer.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Guerbet (Aulnay sous Bois, France) provided the contrast agent used in this study. The authors had control over the data and information submitted for publication, however.

Patient Characteristics
Between February 2004 and October 2004, 48 consecutive patients (mean age, 65.5 years; age range, 51–79 years) from two hospitals in Nijmegen, Gelderland, the Netherlands who had biopsy-proved prostate cancer and were scheduled for pelvic lymph node dissection underwent MR imaging in this prospective study. The patients enrolled in this study had a mean serum prostate-specific antigen level of 23.8 ng/mL (range, 4.3–141.0 ng/mL) and a median Gleason score of 7 (range, 6–10).

Lymphadenectomy was performed at the Radboud University Nijmegen Medical Center, Nijmegen, the Netherlands, or Canisius Wilhelmina Ziekenhuis Nijmegen, Nijmegen, the Netherlands. The inclusion criterion was a serum prostate-specific antigen level higher than 10 ng/mL, a Gleason score of 7 or higher, or the detection of a T3 tumor at digital rectal examination. The exclusion criterion was a positive bone scintigram, having previously undergone androgen therapy, or having previously undergone radiation therapy of the pelvic area. This study was institutional review board approved. Patients were enrolled after they provided written informed consent.

MR Imaging Protocol
For all patients, the cases were numbered and randomized, and their names and the imaging parameters and field strengths used were made anonymous (by R.A.M.H.). This means that all 1.5- and 3.0-T MR images were mixed and presented in random order. Image headers that contained information such as echo time, repetition time, and MR unit type were erased. The imaging data were downloaded onto a personal computer in which Voxar, version 4.2, three-dimensional software (Voxar, Edinburgh, Scotland) was installed.

The patients from both hospitals underwent MR imaging at Radboud University Nijmegen Medical Center. MR imaging was performed by using both 1.5- and 3.0-T MR units (Sonata and TRIO, respectively; Siemens, Erlangen, Germany) and a body and pelvic phased-array coil 24–36 hours after the intravenous infusion of ferumoxtran-10 (Sinerem; Guerbet) (35-nm particle size). Half of the patients were imaged at 1.5 T first, and the other half were imaged at 3.0 T first. Both the 1.5-T and the 3.0-T MR images were acquired within 1 hour. Before both examinations, each patient received an intramuscular injection of 1 mL (20 mg/mL) of butyl scopolamine bromide (Buscopan; Boehringer, Ingelheim, Germany) to reduce peristalsis (11).

After initial localization of the region of interest with gradient-echo imaging in three directions and one coronal fast spin-echo MR measurement with low spatial resolution to plan the section locations, T2*-weighted MR images were acquired by using a multisection two-dimensional gradient-echo sequence with an in-plane resolution of 0.56 x 0.56 x 3.00 mm for 1.5-T imaging and of 0.50 x 0.50 x 2.50 mm for 3.0-T imaging. These images were obtained in a sagittal plane parallel to the psoas muscle (obturator plane) (12). We chose the semisagittal (obturator) plane, because it enables the best view of the lymph nodes along the vessels, which is where most of the nodes are located. Because this plane is parallel to the vessels, it allows optimal differentiation between the vessels and the nodes. Furthermore, urologists have a better understanding of this plane, because it is equivalent to the view that they have at surgery. Finally, with this plane, fewer sections are needed to cover the entire area where the nodes are located; thus, the imaging time can be reduced.

In the two-dimensional T2*-weighted gradient-echo multiecho data image combination sequence, three different echo times are combined and one final image is reconstructed with the mean, or effective, echo time (TEeff). The parameters used in the 1.5- and 3.0-T sequences are presented in Table 1. Before the start of the study, the TEeff of this T2*-weighted sequence was optimized for 3.0-T imaging. To achieve this optimization, the multiecho data image combination sequence was repeated with different TEeff values—12, 15, 18, and 21 msec—in eight patients. The appearances of the nodes on the resulting images were compared with those on the already optimized multiecho combination 1.5-T images. At a TEeff of 21 msec, the loss of signal intensity due to accumulated ferumoxtran-10 extended beyond the edges of the lymph nodes (blooming effect) (13), whereas at a TEeff of 12 msec, there was less darkening of the nodes. Thus, a TEeff of 15 msec was chosen because it yielded the best image quality and a T2* effect comparable to that seen on the 1.5-T images.


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  		Table 1. MR Imaging Parameters

 
Image Interpretation
Three radiologists analyzed the images independently. Each radiologist had experience in evaluating lymph nodes and was familiar with the ferumoxtran-10–enhanced MR imaging criteria for metastatic nodes (4); however, their levels of experience differed. Radiologist 1 (J.O.B.) was the most experienced, with 7 years experience reading ferumoxtran-10–enhanced images and having performed approximately 500 examinations. Radiologist 2 (H.C.M.v.d.B.) had 2 years experience reading ferumoxtran-10–enhanced images and had performed approximately 100 examinations, and radiologist 3 (J.J.F.) had 1 year of experience interpreting ferumoxtran-10–enhanced MR images and had performed approximately 50 examinations. The readers were blinded to the biochemical parameters used and were free to adjust the window and level settings.

A questionnaire was designed for use in collecting all data. The following image parameters were assessed by using a five-point scale: muscle-fat contrast, vessel-fat contrast, and lymph node border delineation. The scores on the five-point scale were as follows: 1 for very poor, 2 for poor, 3 for adequate, 4 for good, and 5 for very good. No specific criteria for each point on the scale were used. Motion artifacts that degraded the images also were assessed by using a five-point scale, on which 1 meant severe and 5 meant absent. The subjective overall image quality was measured by using a 10-point visual analogue scale (VAS) score as the general indicator of diagnostic quality. After all questionnaires were completed, they were collected and decoded for further statistical analysis.

Statistical Analyses
Statistical analyses were performed by using computer software (SPSS, version 12.0.1; SPSS, Chicago, Ill). All reported P values were derived by using two-sided tests in which P ≤ .05 indicated a statistically significant difference. First, the Mann-Whitney U test was performed to compare the mean image parameter scores assigned at 1.5- and 3.0-T MR imaging and to calculate the significance of the differences. However, the Mann-Whitney U test does not enable one to distinguish between multiple factors such as patient, reader, and MR technique (ie, 1.5 or 3.0 T). Therefore, to estimate the degree of contribution of certain factors to the variability of the results, a second test, the general linear mixed model test (14), was applied. Muscle-fat contrast, vessel-fat contrast, lymph node border smoothness, motion artifacts, and VAS score were separately regarded as dependent variables. The patient, the reader, and the MR imaging technique used (ie, 1.5 or 3.0 T) were considered random factors. The contributions of these factors and of the interactions between these factors to the variability of the results were calculated.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
For all dependent variable scores, mean values were calculated (Table 2). All dependent variable scores improved significantly at 3.0 T (P < .05, Mann-Whitney U test). The percentage contributions of the three random factors—patient, reader, and technique—indicated that the factor of patient, alone or in interaction with one or more other random factors, appeared to contribute little variance to the observed dependent variable scores (Table 3). The greatest proportion of variance in the scores for the dependent variables motion artifacts and muscle-fat contrast (Figure, Tables 3, 4) could be attributed to the MR imaging technique used.


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  		Table 2. Mean and Median Scores for Dependent Variables on 1.5- and 3.0-T MR Images

 

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  		Table 3. Percentage Contributions of Random Factors to Variability in MR Image Dependent Variable Scores

 

Figure 1
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  		Figure a: Ferumoxtran-10–enhanced T2*-weighted gradient-echo (a) 1.5-T (voxel size, 0.56 x 0.56 x 3.0) and (b) 3.0-T (voxel size, 0.50 x 0.50 x2.5) MR images (obturator plane) in 63-year-old man with prostate cancer (Gleason score, 7; serum prostate-specific antigen level, 19 ng/mL; digital rectal examination result, stage T2b). The improved image quality on b is a result of decreased motion artifacts, improved muscle-fat contrast, improved vessel-fat contrast, and improved lymph node border delineation (circles). The signal intensity of the bone marrow (arrows) is lower at 3.0 T owing to increased T2* effects.

 

Figure 1
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  		Figure b: Ferumoxtran-10–enhanced T2*-weighted gradient-echo (a) 1.5-T (voxel size, 0.56 x 0.56 x 3.0) and (b) 3.0-T (voxel size, 0.50 x 0.50 x2.5) MR images (obturator plane) in 63-year-old man with prostate cancer (Gleason score, 7; serum prostate-specific antigen level, 19 ng/mL; digital rectal examination result, stage T2b). The improved image quality on b is a result of decreased motion artifacts, improved muscle-fat contrast, improved vessel-fat contrast, and improved lymph node border delineation (circles). The signal intensity of the bone marrow (arrows) is lower at 3.0 T owing to increased T2* effects.

 

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  		Table 4. MR Image Dependent Variable Scores for a Specific Patient

 
For muscle-fat contrast, 40.7% of the increase in mean score, from 3.03 at 1.5 T to 3.83 at 3.0 T, could be attributed to the difference in MR imaging technique—that is, the use of a 3.0-T MR unit. The interaction between reader and technique made relatively large contributions to the variance in scores for the dependent variables lymph node border delineation and VAS score: 31.6% and 34.1%, respectively. This finding indicates that some but not all of the readers observed a systematic difference in lymph node border delineation and VAS score between 1.5- and 3.0-T imaging. After evaluation of the raw data, it appeared that this discrepancy was due to one deviating reader (radiologist 3).

A separate variance components analysis was performed with the deviating reader excluded. At this analysis, a shift from the reader-technique interaction to the technique as the large contributor to the variance in scores was observed. The percentage contributions of the technique to the variance in scores for lymph node border delineation and VAS score now increased from 18.2% to 45.2% and from 19.1% to 45.5%, respectively (Table 5). The percentage contributions of the reader-technique interaction to the variance in these scores decreased to 5.1% and 5.7%, respectively (Table 5). These findings indicate that for all readers, the significantly decreased motion artifacts and improved muscle-fat contrast were the results of using the 3.0-T technique (Tables 2, 3), whereas for two readers, this was also true for the improved lymph node border delineation and VAS score (Table 5).


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  		Table 5. Percentage Contributions of Random Factors to Variability in MR Image Dependent Variable Scores, with Exclusion of Deviating Reader

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
 References
 
Our study results show that ferumoxtran-10–enhanced MR images of pelvic nodes can be obtained at 3.0 T. Furthermore, the image quality at 3.0-T MR imaging was improved compared with that at 1.5-T MR imaging owing to fewer motion artifacts according to all readers and owing to better lymph node border delineation according to two readers.

Previous study investigators have described how ferumoxtran-10–enhanced MR imaging improved the staging of pelvic lymph nodes in prostate cancer (4,6). Use of the ferumoxtran-10–enhanced MR technique has resulted in superior outcomes compared with the outcomes of using other cross-section modalities such as computed tomography and nonenhanced MR imaging (15–19). These techniques involve the use of only the size (8–10 mm) and shape (round or oval) criteria described by Jager et al (12) and therefore are limited. Harisinghani et al (4) achieved a sensitivity of 100% and a specificity of 96% for detection of 5–10-mm nodes at 1.5 T. However, when the metastatic lymph node was smaller than 5 mm, the sensitivity decreased to 41%. In prostate cancer, metastases are found predominantly in these very small nodes. This could explain why some positive lymph nodes are still missed when the technique of Harisinghani et al is used.

A higher signal-to-noise ratio enables imaging with a higher spatial resolution. In our study, use of the same acquisition time resulted in a higher spatial resolution and thinner sections and thus improved image quality. Lymph node delineation in particular improved at 3.0 T, with fewer motion artifacts. This improvement in image quality could affect the detection threshold of 5 mm. In other words, it probably could enable the detection of smaller metastases in smaller nodes or the detection of smaller focal metastases in large nodes. Future studies of ferumoxtran-10–enhanced MR imaging at 3.0 T will be performed to evaluate the potential improved detection of micrometastasis with this technique and to assess the associated diagnostic accuracy.

Our study was designed to enable one to obtain optimal results at both 3.0 T and 1.5 T during equivalent acquisition times. However, the TEeff values at 1.5- and 3.0-T imaging are different. The TEeff at 3.0 T was reduced to 15 msec. We expected the susceptibility artifacts at 3.0-T imaging to be increased compared with those at 1.5-T imaging, meaning that the T2* blooming effect (13) with use of the same TEeff would be substantially greater at 3.0 T. Such an effect may overshadow a small metastatic lesion. Therefore, to achieve an equal susceptibility effect, we decided to optimize the TEeff in eight patients before beginning this study. Only a small decrease in TEeff, from 18 msec at 1.5 T to 15 msec at 3.0 T, was required and resulted in better delineation of the nodes. It is important to realize, however, that the real effect of using 3.0-T imaging cannot be evaluated until robust models for nodal patterns of metastases are compared between the 1.5- and 3.0-T systems. The size of metastases and the susceptibility seen at 3.0-T imaging need to be considered. Nodal metastases of varying sizes need to be evaluated at different echo times to determine which values are suitable for optimal detection without spillover susceptibility. Additional sequence optimization could further improve the results of 3.0-T MR imaging.

Another imaging modality that depicts lymph nodes is PET. PET scanning with fluorine 18 fluorodeoxyglucose is very promising in lung cancer assessment (20). However, because of the low metabolic activity of prostate cancer, PET is not sensitive enough to depict small lymph nodes (7,21–23). It is possible that the use of new tracers will help to overcome this problem. de Jong et al (7) reported that current PET cameras have a low intrinsic spatial resolution of 5 mm and therefore are not useful for imaging microscopic disease. Because of the low signal-to-noise ratio, the newer generations of cameras with a spatial resolution of 2 mm will not improve these results (7).

The general linear mixed model was used to determine which factors had the greatest effect on the imaging results. After the first statistical general linear mixed model analysis, one radiologist (reader 3) was excluded. The relatively low level of experience, the given reading, and/or deviating interpretations of the instructions probably contributed to the deviation of this reader's findings from the other two readers' findings.

High-magnetic-field-strength (3.0-T) MR imaging units are increasingly becoming available throughout the world. MR imaging at 3.0 T is a valuable tool for neurologic imaging (8,9). However, in whole-body MR imaging, specific absorption rate problems often limit the conversion of sequences from 1.5 to 3.0 T. In this study, no specific absorption rate problems were encountered. Specific absorption rate limitations appear especially when numerous radiofrequency pulse sequences with a large flip angle and a short repetition time, such as fast spin echo, are used but not when low-angle pulse sequences, such as gradient echo, are used. In our study, the specific absorption rate had no influence because only gradient-echo sequences with a flip angle of 36° were used.

In terms of limitations, there are conflicting literature reports on the dielectric effects of using a higher magnetic field strength. Some study results indicate that image degradation occurs (24–27), while others report that this effect occurs in water phantoms only and is absent in human imaging (26). In the current study, we observed no effect related to this phenomenon; the image quality was actually judged to be better at 3.0 T. This may have been the result of using a body phased-array coil. Despite all of the reported promising study results, ferumoxtran-10 currently is not approved for use in the United States or Europe.

In conclusion, the outcomes obtained in our study indicate that it is feasible to perform ferumoxtran-10–enhanced MR imaging at a magnetic field strength of 3.0 T—and thus with a higher spatial resolution—and achieve improved image quality compared with the image quality achieved at 1.5 T. This improved image quality may enable the detection of small (<5 mm) metastatic lymph nodes in the future.


   ADVANCES IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
References
 


   FOOTNOTES
 

Abbreviations: TEeff = effective echo time • VAS = visual analogue scale

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, all authors; 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, R.A.M.H., T.W.J.S.; clinical studies, R.A.M.H., H.C.M.v.d.B., J.O.B.; experimental studies, R.A.M.H., T.W.J.S., J.O.B.; statistical analysis, R.A.M.H., A.M.H.; and manuscript editing, all authors


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 

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